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Global perspectives on the ecological, cultural and socioeconomic relevance of wild edible fungi

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  • Wild edible fungi (WEF), including mushrooms and truffles, comprise a natural source of nutritious and healthy food. The consumption of WEF began at least 18, 700 years ago during the Stone Age. Current data from over 100 countries indicates the existence of more than 2, 100 edible species, a figure that is continually growing, as vast regions and many cultures remain understudied. However, only around 30 species of WEF are grown commercially at a large-scale. WEF also play a key ecological role in the structure and functioning of natural ecosystems and have significantly contributed in shaping all life on the planet. Either as food, medicine or both, they are important for the survival, cultures, and economies of hundreds of ethnic groups around the globe. Over the last 15 years, there has been a noteworthy increase in the international trade of WEF, which is currently estimated at billions (USD) annually. In 2017, the WEF global trade, of either fresh or processed products, exceeded 1, 230, 000 tonnes. Due to their ecological, sociocultural and economic importance, the international WEF trade has a role to play in the postpandemic recovery period. The main challenge of this period will be maintaining natural ecosystems while simultaneously improving human wellbeing. Critical elements of this challenge include ensuring food security, enhancing rural development, creating sustainable jobs, mitigating hunger, and slowing the loss of traditional knowledge generated over millennia. This review analyzes the ways in which sustainable use of WEF could contribute to achieving these goals.
  • Phoebe bournei, a rare and endangered protected tree species that is unique to China, which produces excellent material and fragrance, can be used for the production of furniture and as an ornamental tree[1] . However, few natural resources of this species are available, and this species undergoes a long juvenile phase. Currently, seed propagation is the main reproduction technique, and unstable yields driven by fruiting characteristics has a large impact on seedling production[2].

    Somatic embryogenesis (SE) is one of the most important techniques for tree breeding programs, but the mechanism underlying SE is poorly understood[3]. In angiosperms, a mature somatic embryo is induced from embryonic calli and subsequently develops into spherical, heart-shaped, torpedo, and cotyledon-producing embryos[4]. Moreover, regulation of the different stages of SE requires specific cell fate changes, and many transcription factors (TFs) are involved in this process. For example, WUSCHEL (WUS), WUSCHEL-related homeobox (WOX), BABY BOOM (BBM), AGAMOUS-like (AGL), LEAFY COTYLEDON (LEC), Receptor-Like Kinase (SERK), and Vmyb Avian Myeloblastosis Viral Oncogene Homolog (MYB) genes function as indispensable regulators transforming nonembryogenic calli cells into embryogenic calli cells or driving changes between the different developmental stages of SE[510]. As such, SE requires precise transcriptional regulation. SE regeneration techniques have been determined for P. bournei[11], and high-quality genomic data of this species have been released by our group[12]. However, the transcriptional regulatory mechanism behind the transitions among the different stages of SE in P. bournei remains elusive.

    An increasing number of studies have shown that WOXs are extensively involved in plant organ regeneration, growth and development, stress responses, and other transcriptional regulatory processes, especially those that occur during SE[1317]. In Arabidopsis, AtWUS was shown to be expressed at the proembryonic (16-cell) stage and is involved in subsequent maturation during SE[18]. AtWOX2, AtWOX8, and AtWOX9 participate in polarity establishment during early embryonic development, and AtWOX2 is expressed in apical cells, while AtWOX8 and AtWOX9 are expressed specifically in basal cells, which are indispensable for the correct establishment of the apical–basal axis[19,20]. Moreover, PaWOX2 was also shown to be highly expressed in embryogenic cells in Picea abies[21], and the overexpression of PpWOX2 was shown to affect related traits of somatic embryos in Pinus pinaster[17]. In Vitis vinifera, VvWOX2 and VvWOX9 are expressed at high levels during SE and can be used as marker genes for SE[22]. Furthermore, MtWOX9-1 was shown to increase the embryogenic capacity of recalcitrant plant species, e.g., Medicago truncatula[23]. These studies have shown that WOXs are crucial during the process of embryonic development or somatic embryo regeneration. Moreover, in woody plant species, global transcriptomic data and expression analysis have resulted in the identification of WOXs expressed during SE in Dimocarpus longan, hybrid sweetgum, and Elaeis guineensis, suggesting that WOXs are functionally conserved in woody plants species[7,9,24]. Based on this, understanding the dynamic relationship between WOXs and SE in P. bournei is helpful for optimizing the somatic embryo regeneration system and creating a large number of clones rapidly.

    Previous studies have shown that overexpression or ectopic expression of embryogenesis-related TFs can induce the SE process. Another way is to apply exogenous phytohormones[25]. Adding exogenous phytohormones to media can affect the morphology and quality of SE in many species[26]. The interactions between phytohormones and TFs has been under increasing scrutiny. Several studies have shown that some TFs, such as LEC2, BBM, and WUS, are regulated by auxin synthesis, transport, and responses during SE[10,27,28]. Correct establishment of the auxin gradient and PIN1-mediated auxin transport were shown to affect the expression level of WUS, which in turn affected the status of the embryonic calli[27]. LEC2 and BBM transcriptionally regulate the endogenous auxin (IAA) biosynthesis-related genes YUCs/TAAs and increase the DR5 auxin response, further maintaining somatic embryo growth[10,28,29]. Furthermore, LEC2 was shown to bind directly to the early embryonic marker genes WOX2 and WOX3, triggering SE[5,25]. Abscisic acid (ABA) is another important hormone involved in SE, especially during embryo maturation. Application of exogenous ABA to the media was shown to induce embryo maturation and prevent early germination in Carica papaya, Pseudotsuga menziesii, and Phoenix dactylifera[3032]. Methyl jasmonate (MeJA) plays a function similar to that of ABA in promoting mature SE. MeJA functions synergistically with ABA, but the effects of MeJA cannot replace the effects of ABA[33]. In Liriodendron hybrids, MeJA was shown to increase both SE and the maturation rate and decreased the deformation rate[34]. However, studies on the relationships between MeJA and WOXs are lacking. Taken together, these results suggested that TFs and hormones jointly regulate plant SE. In P. bournei, how WOXs respond to hormones during SE has not been thoroughly characterized. So we preliminarily explored the expression patterns of WOX under auxin, ABA, and MeJA treatments.

    In the present study, 15 WOX genes were identified across the P. bournei genome, and their gene structures and protein sequences were characterized. Then, the expression patterns of WOXs among six tissues and at different stages of SE were determined. To elucidate how these WOXs respond to hormones, their expression levels in response to auxin, ABA, and MeJA were analyzed. Our results revealed WOX members in P. bournei and several possible associations between WOXs and plant hormones. The results of this study will provide further insight into the function of WOXs involved in regulating SE in woody plant.

    The half-sibling family of P. bournei designated 'WY1' was cultivated in the greenhouse. The epicotyls, stem tips, roots, stems, and leaves of three-month-old seedlings and embryogenic calli induced from immature embryos were frozen in liquid N2 and used for semiquantitative analysis of PbWOX genes. Growth of embryonic calli was induced in cotyledon-stage embryos of the 'WY1' mother tree and subcultured at 24 °C in the dark, as described in our previous study[11]. Somatic embryos of P. bournei at six developmental stages, including three stages of calli, the globular embryo stage, and immature and mature cotyledon-producing embryo stages, were collected under a stereomicroscope (OLYMPUS, Beijing, China) and then frozen in liquid N2 for RNA extraction. With respect to calli growth in liquid media for hormone treatment, 0.1 g of calli was transferred to liquid media supplemented with 100 μM IAA, ABA, and MeJA for 3, 6, 12, 24, and 48 h. Calli in untreated liquid media were used as controls. Sampling was performed at the same time, and three replicates were included.

    The PbWOXs were identified by two methods. Firstly, using the hidden Markov model, we downloaded the sequence of the conserved homeobox domain of the WOX (PFAM00046) from an online website (http://pfam.xfam.org), and the hmm search module in HMMER (version 3.1) software was used to search the protein sequences of the P. bournei genome[12]. The threshold was set to < E20. Secondly, we downloaded 15 AtWOXs proteins sequence from the TAIR database (www.arabidopsis.org), then used them as query sequences to perform the BLASTp search (E-value < 1e-5) with P. bournei protein sequences. By combining the two methods, candidate sequences without a homeobox domain were omitted. The 15 obtained PbWOX protein sequences were subjected to MUSCLE alignment of MEGA (version 7.0) together with the sequences of 15 AtWOXs, 13 OsWOXs, 18 PtWOXs, eight AtriWOXs, seven SmWOXs, three PpaWOXs, one OstuaWOX, and one OstluWOX protein downloaded from the online Plant Transcription Factor Database (PlantTFDB) website (http://planttfdb.cbi.pku.edu.cn). The neighbor-joining (NJ) method with 1000 bootstrap repetitions was subsequently used to construct a phylogenetic tree, and the other parameters were set to their default.

    Exons and introns of individual PbWOXs were visualized via the online software Gene Structure Display Server (GSDS) (version 2.0) (http://gsds.gao-lab.org), and Multiple Em for Motif Elicitation (MEME) (version 5.11) (http://meme-suite.org/) was used to predict the motifs of the PbWOX family proteins. The ProtParam (https://web.expasy.org/protparam/) online website was subsequently used to predict the physicochemical properties of PbWOX family members, such as their number of amino acids, molecular weight, and isoelectric point. ClustalX (version 1.81) was used for multiple sequence alignment to confirm the presence of WUS-box domain and the homeobox domain. The genome sequence and gene annotation information file was added to the TBtools GFF3 Sequence Extractor submenu, the upstream bases was set to 2000, the upstream CDS 2.0 kb of all genes in P. bournei were obtained. Then 2.0 kb upstream promoter sequences of 15 PbWOX genes were obtained from the TBtools quick fasta extractor submenu[12,35]. Finally, we uploaded the obtained file to an online site PlantCARE (http://bioinformatics.psb.ugent.be/webtools/plantcare/html/) to analyze cis-acting elements.

    Total RNA was extracted using a RNAprep Pure Plant Kit (TIANGEN, Beijing, China). Then, the RNA was quantified by a Nanodrop ND-1000 spectrophotometer and checked according to the A260/280 nm and A260/A230 nm values. Subsequently, cDNA was synthesized using a PrimeScriptTM RT Reagent Kit with gDNA Eraser (Perfect Real Time) (Takara, Dalian, China), and each RNA sample was 2000 ng. The obtained cDNA was subsequently diluted five times for quantitative RT‒PCR.

    Specific primers of the 15 PbWOX genes were designed using the Primer 3 online website (http://bioinfo.ut.ee/primer3-0.4.0/), and the sequences of these primers are listed in Supplemental Table S1. The expression levels of the PbWOX genes were detected via quantitative RT–PCR and a CFX 96-well Real-Time PCR System (Bio-Rad, USA). The qPCR mixture volume was 10 μL, which comprised 5 μL of 2× ChamQTM SYBR qPCR Master Mix, 0.4 μL of cDNA, 0.2 μL of forward primer, 0.2 μL of reverse primer, and 4.2 μL of ddH2O. The PCR was carried out as follows: predegeneration at 95 °C for 1 min, 45 cycles of denaturation at 95 °C for 10 s followed by annealing at 57 °C for 10 s, and extension at 72 °C for 20 s. PbEF1α was used as an internal control, and the relative gene expression levels were calculated according to the 2−ΔΔCᴛ method[36].

    All the treatments were performed at least three times. The data were subjected to ANOVA and Duncan's multiple range test at the 5% significance level via SPSS (version 26.0) software.

    After performing hidden Markov model (HMM) searches and removing redundant and/or sequences without the homeobox domain, we identified 15 PbWOX members. Phylogenetic analysis of 15 AtWOXs, 18 PtWOXs, 13 OsWOXs, eight AtriWOXs, seven SmWOXs, three PpaWOXs and WOX protein sequences from two green algal species resulted in the assignment of the 15 PbWOX genes to an ancient branch, an intermediate branch and a modern/WUS branch (Table 1). Specifically, the ancient branch consisted of three PbWOXs (PbWOX13a, PbWOX13b, and PbWOX13c); the intermediate branch consisted of four PbWOXs, namely, PbWOX9, PbWOX11/12a, PbWOX11/12b, and PbWOX11/12c, which were classified into two subclasses; and the remaining eight members, namely PbWUS, PbWOX1a, PbWOX1b, PbWOX2a, PbWOX2b, PbWOX3, PbWOX4 and PbWOX5/7, were assigned to the modern/WUS branch (Fig. 1a).

    Figure 1.  Phylogenetic relationships of PbWOX proteins. (a) NJ tree constructed of the amino acid sequence of WOXs from Phoebe bournei (Pb), Arabidopsis thaliana (At), Populus trichocarpa (Pt), Oryza sativa (Os), Amborella trichopoda (Atri), Selaginella moellendorffii (Sm), Physcomitrella patens (Ppa), Ostreococcus tauri (Ostau) and Ostreococcus lucimarinus (Ostlu). (b) Synteny analysis of WOX genes between P. bournei and A. thaliana. Gray lines indicate all synteny blocks in the genome, and the red lines indicate duplicated WOX gene pairs.
    Table 1.  Subclass information of WOXs among P. bournei and other representative species.
    Taxonomic groupSpeciesAncient cladeIntermediate cladeModern/ WUS
    clade
    Total
    DicotsA. thaliana34815
    P. trichocarpa671118
    MonocotsO. sativa16613
    MagnolialesP. bournei34815
    AmborellalesA. trichopoda1258
    PteridophytaS. moellendorffii617
    BryophytaP. patens33
    ChlorophytaO. tauri11
    O. lucimarinus11
     | Show Table
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    However, the number of PbWOX genes was the same as that of Arabidopsis (Fig. 1a). Nonetheless, PbWOXs probably expanded differently than did those of Arabidopsis. For example, three homologs of AtWOX11/12 and AtWOX13, two homologs of AtWOX1 and AtWOX2, one homolog each of AtWUS, AtWOX3, AtWOX4, AtWOX5/7, and AtWOX9, and no homologs of AtWOX6 and AtWOX10 were found in P. bournei (Fig. 1b).

    A sequence analysis of the PbWOXs showed that PbWOX1b comprised the largest number of amino acid residues (528) and had the largest molecular weight (59.19 kD). Conversely, PbWOX5/7 comprised 169 amino acid residues and had the smallest molecular weight (19.37 kD). All PbWOX genes contain introns, the number of which ranged from two to eight (Fig. 2a). Then, to better understand each member of the PbWOXs, we predicted the physicochemical properties by the use of an online website. The theoretical isoelectric point of PbWOX was found to be between 5.48 (PbWOX11/12c) and 9.93 (PbWOX13c) (Table 2).

    Figure 2.  Information on the PbWOX genes and proteins. (a) Phylogenetic tree and gene structure. (b) Architecture of conserved protein motifs. (c) Multiple sequence alignment.
    Table 2.  Summary of the PbWOX gene family members.
    Gene IDGene nameOrthologous in ArabidopsisTheoretical pIMolecular weightNumber of amino acids
    OF24054-RAPbWUSAtWUS8.5831622.96276
    OF03970-RAPbWOX1aAtWOX19.3737209.6328
    OF11837-RAPbWOX1bAtWOX18.8959188.97528
    OF19048-RAPbWOX2aAtWOX27.0924524.5218
    OF05256-RAPbWOX2bAtWOX26.8324496.61219
    OF16243-RAPbWOX3AtWOX39.0522752.66194
    OF04424-RAPbWOX4AtWOX48.2524797.85220
    OF05362-RAPbWOX5/7AtWOX5, AtWOX79.5119371.68169
    OF24594-RAPbWOX9AtWOX97.1945272.57413
    OF22069-RAPbWOX11/12aAtWOX11, AtWOX125.6830055.89268
    OF11766-RAPbWOX11/12bAtWOX11, AtWOX125.9530330.35277
    OF28194-RAPbWOX11/12cAtWOX11, AtWOX125.4827450.91252
    OF25757-RAPbWOX13aAtWOX135.9132705.61288
    OF14063-RAPbWOX13bAtWOX136.1032380.27286
    OF07768-RAPbWOX13cAtWOX139.9331294.66272
     | Show Table
    DownLoad: CSV

    Motif 1 and motif 2 were detected in all 15 PbWOXs, motif 3 was specific to the members of the intermediate clade, motif 4 (T-L-X-L-F-P-X-X, where X indicates any amino acid) was present in all members of the modern/WUS clade except PbWOX5/7, and motif 5 was specific to PbWOX13a and PbWOX13b (Fig. 2b). There are residues composing homeobox domain motifs that contain three helixes spaced by one loop and one turn (Fig. 2c). Eight members in the modern/WUS clade shared a WUS-box domain (Fig. 2c).

    The cis-acting elements in the promoter region of PbWOXs were divided into four main categories: light-related, hormone-related, stress-related and development-related. (Fig. 3). Specifically, the light response elements constituted the largest proportion, of which the number of G-box elements was the largest. Several other elements involved circadian rhythm were also detected. The hormone-responsive elements included 45 ABA-responsive elements (ABREs), 30 MeJA-responsive elements (CGTCA motif–containing elements), 24 gibberellin (GA)-responsive elements (P-boxes, GARE motif–containing elements, TATC-boxes), 10 salicylic acid-responsive elements (TCA-elements), and nine auxin-responsive elements (TGA-elements, AuxREs, AuxRR-core elements). Abiotic stress response elements were predicted with 38 regulatory anaerobic inductor elements (ARE), 20 drought-responsive elements that could bind MYBs (MBSs), 15 low-temperature–responsive elements (LTRs), eight defense- and stress-responsive elements and five anoxic-specific induction-responsive elements. Moreover, in development-related cis-acting elements, 14 CAT boxes, 12 O2-sites, and six RY elements were predicted, respectively. In the PbWOX promoters, the most common cis-acting elements were G-boxes (light-related), ABREs (ABA-related), CGTCA motif-containing elements (MeJA-related) and AREs (drought-related). This result implied that PbWOX participated in plant growth process and stress response.

    Figure 3.  Predicted cis-acting elements in PbWOX promoters. (a) Frequency of cis-acting elements in the 2.0 kb upstream regions of PbWOXs. The corresponding colored bar chart indicates the occurrence of different cis-acting elements. (b) Number of cis-acting elements in each WOX gene.

    To further understand the potential roles of PbWOXs during different developmental stages and at different physiological status, semi-qPCR was used to study the expression patterns of 15 PbWOXs in six tissues. The expression levels of PbWOXs varied significantly among the tissues (Fig. 4). Specifically, five genes, namely, PbWOX2a, PbWOX5/7, PbWOX9, PbWOX13a, and PbWOX13b, were expressed in almost all the tissues, while PbWUS, PbWOX1a, PbWOX2b and PbWOX3 were highly expressed in the epicotyls, with low or no expression in the other tissues. In addition, PbWOX11/12a, PbWOX11/12b and PbWOX11/12c were highly expressed specifically in both the roots and embryogenic calli, while expression of PbWOX1b and PbWOX4 was nearly absent in the calli. In total, nine PbWOXs were expressed in embryogenic calli, and thus, these genes may be involved in the SE of P. bournei; PbWOX2a exhibited the highest expression level.

    Figure 4.  Semiquantitative analysis of PbWOXs in different tissues. (a) Tissue samples, 1 - epicotyl, 2 - stem tip, 3 - root, 4 - stem, 5 - leaf, 6 - calli. (b) Semiquantitative PCR electropherogram.

    Previous studies have shown that WOXs play important roles during SE. The expression levels of nine PbWOXs were analyzed in calli at three different developmental stages (Fig. 5ac) and in embryos at three different developmental stages (Fig. 5dg). Embryonic calli were induced by immature zygotic embryos (Fig. 5a); then, the embryonic calli developed to the second stage (Fig. 5b) after two or three rounds of propagation, and the calli developed to the third stage (Fig. 5c) after two rounds of propagation. Globular embryos (Fig. 5d), immature cotyledon-producing embryos (Fig. 5e) and mature cotyledon-producing embryos (Fig. 5f) were also selected. The qPCR results showed that the expression levels of PbWOX2a and PbWOX9 increased during embryogenic calli development but decreased as the embryos matured. PbWUS was specifically and highly expressed in the immature cotyledon-producing embryos. The expression level of PbWOX5/7 increased during calli development but decreased after calli differentiation. Three homologous genes, PbWOX11/12 and PbWOX13a, were highly expressed in cotyledon-producing embryos, and their expression peaked upon maturity (Fig. 5g).

    Figure 5.  Expression patterns of PbWOXs during SE of P. bournei. (a) Calli-1. (b) Calli-2. (c) Calli-3. (d) Globular embryo. (e) Immature cotyledon-producing embryo. (f) Mature cotyledon-producing embryo. (g) Analysis of gene expression via qPCR. The data are the means ± SDs of three biological replicates. The values followed by the same letter are not different according to Duncan’s multiple-range test. PbEF1α was used as an endogenous control.

    With respect to the cis-acting elements of PbWOXs, we investigated the expression patterns of PbWOXs in response to auxin, ABA, and MeJA (Fig. 6). Under IAA treatment, PbWUS expression was induced and increased continuously as the treatment duration increased; PbWOX5/7 was strongly induced after 3 h of treatment, after which the expression level decreased. The expression levels of PbWOX2a and PbWOX9 significantly decreased, and the expression levels of PbWOX11/12b, PbWOX11/12c, PbWOX13a, and PbWOX13b also slightly decreased.

    Figure 6.  Relative expression levels of PbWOXs under hormone treatment. The data are the means ± SDs of three biological replicates. The values followed by the same letter are not different according to Duncan's multiple-range test. PbEF1α was used as an endogenous control.

    PbWUS was also induced in response to ABA treatment, while PbWOX2a, PbWOX9, and PbWOX13b were inhibited. The expression levels of PbWOX5/7 and PbWOX13a decreased, reached their lowest level after 12 h of ABA treatment, and then gradually increased. PbWOX11/12b and PbWOX11/12c showed similar expression patterns; their expression increased after 3 h but then decreased. PbWUS expression was induced in response to MeJA treatment, peaked at 12 h, and then gradually decreased. PbWOX5/7, PbWOX9 and PbWOX13b expression was inhibited significantly. PbWOX11/12b and PbWOX11/12c expression increased after 3 h but then decreased.

    WOXs are specific to plants and largely involved in key developmental processes, especially those associated with somatic cell regeneration. With the publication of many plant genome sequences, WOX genes have been identified in several plant species. In the present study, we identified 15 PbWOXs, same as the number in Arabidopsis[37], and different orthologous revealed that chromosomal duplication events may occur in P. bournei. Furthermore, the length of introns showed regular characteristics across different clades. For instance, genes in the intermediate clade contained shorter intron sequences than did those of ancient clade, and five genes in the modern/WUS clade had the shortest intron. Taken together, these results suggested that the intron fragments underwent refinement during the evolution of the PbWOX genes. A similar phenomenon was observed in Camellia sinensis[38], which was exemplified by most WOX introns in members of the modern/WUS clade are much shorter than those in the ancient clade. In addition, compared with that in algae, ferns and other more ancestral plant species with one or two members, the WOX family gene in woody plant species has expanded in number and evolved in terms of sequence.

    Tissue-specific expression of a gene implies that the gene plays an indispensable role in certain tissues. We found that, like those in Arabidopsis, the WUS genes in P. bournei were mainly expressed in the epicotyls and shoot apical meristems (SAMs), but this is unlike the patterns of other popular genes, which are expressed in the SAMs, roots, stems, and leaves[39]. These results suggested that PbWUS might play a crucial role in maintaining the differentiation of the SAM. In Arabidopsis, AtWOX4 participates in TDIF-TDR-WOX4 signaling to maintain vascular meristem organization during secondary growth[40], which is similar to what occurs in poplar[41,42]. Here, PbWOX4 was also highly expressed in the stems; thus, this gene may have a function in P. bournei like that of its homologs in Arabidopsis and poplar. In addition, PbWOX4 was also expressed in the roots, leaves, and other plant tissues except embryogenic calli, suggesting that this gene is not involved in plant regeneration or development in vitro. Like AtWOX11, PtoWOX11/12a, and PtoWOX11/12b, three members, namely, PbWOX11/12a, PbWOX11/12b, and PbWOX11/12c, were expressed in the roots and embryogenic calli. Previous studies have shown that WOX11 is involved in adventitious root formation, which has an essential function in root regeneration during de novo plant regeneration[4346]. Therefore, it was speculated that these three PbWOX11 members might participate in calli propagation and/or root regeneration in P. bournei.

    SE is one of the important mechanisms of plant asexual reproduction and is subject to complex transcriptional regulation, which in turn enables precise cell fate transitions and the formation of a complete plant. This hierarchical transcriptional regulatory network structure for SE has been revealed in Arabidopsis; in this process, WOX2 and WOX3 are the key TFs that induce SE[5]. According to the tissue expression patterns among tissues, we identified nine WOX genes that were expressed in embryogenic calli—the early stage of SE.

    WUS plays a crucial role in embryogenesis by promoting the fate of cells to transform and develop into embryos, and WUS can also drive the activity of embryonic stem cells. An earlier study showed that WUS is expressed in the four inner apical cells of 16-cell embryos and promotes the formation of the SAM during embryo development, and overexpression of WUS promotes the formation of high-frequency SE. Like in other species, such as Coffea canephora[47], Medicago truncatula[48], and Gossypium hirsutum[15], WUS overexpression resulted in an increased SE induction ratio. In our study, the expression level of WUS significantly increased in the late stage of embryogenic calli and increased significantly again at the immature cotyledon-producing embryo stage. These results indicated that PbWUS promotes the proliferation of embryogenic calli, affects the establishment of cell axial polarity, such as the formation of apical bud meristems during embryonic development in plants, and especially promotes the transition to cotyledon-producing embryos.

    In addition to WUS, WOX2 and WOX9 are the most reported WOX genes involved in plant SE. In the present study, PbWOX2a and PbWOX9 exhibited similar expression patterns, which were exemplified by higher expression levels observed at the embryogenic cell stage and during early somatic embryo formation. In Arabidopsis, it has been proposed that AtWOX2 and AtWOX9 play crucial roles in apical–basal axis formation during embryo development[19]. AtWOX2 is expressed in the apical cell, whereas AtWOX9 is expressed in the basal cell. These genes expressed at specific sites drive the fate of cells in the embryo. In grapevine, both VvWOX2 and VvWOX9 are labeled marker genes of early embryogenic phases[22]. In addition, WOX2 and WOX9 were found to play crucial roles in the early stage of SE in the gymnosperm Picea abies[21,49]. Therefore, PbWOX2a and PbWOX9 might be marker genes for early embryonic development of P. bournei.

    WOX11 has been reported to be an important upstream gene involved in the generation of root system architecture and to promote adventitious root formation during de novo root organogenesis from leaf explants[44,50], but this gene has not been found to be related to root regeneration in plant SE. We noted that PbWOX11/12a, PbWOX11/12b, and PbWOX11/12c were all detected in the embryogenic calli, specifically in immature and mature cotyledon-producing embryos. A similar phenomenon has been observed in grapevine, exemplified by VvWOX11 being highly expressed in torpedo-stage and cotyledon-producing embryos[22]. These findings further support that WOX11/12 might play an important role in the later stage of somatic embryo development and is probably related to root development, but whether WOX11/12 is involved in root primordium formation remains to be confirmed.

    In P. bournei, two WOX13 genes orthologous to AtWOX13 were detected in calli and somatic embryos, but their expression patterns differed. The expression level of PbWOX13a gradually increased with embryo development, while that of PbWOX13b showed no significant change. To our knowledge, WOX13 is expressed ubiquitously and participates in calli formation and organ reconnection in Arabidopsis[51]. However, the molecular regulatory roles of WOX13 during somatic embryo regeneration remain unclear, and expression profiles have been reported in only Vitis vinifera, in which three VvWOX13 genes exhibited low expression levels in somatic embryos, and the expression profile was unaffected by environmental changes[22]. Our data showed that two PbWOX13s also exhibited ubiquitous expression patterns. Nevertheless, PbWOX13b expression seemingly changed nonsignificantly during embryonic calli induction and mature cotyledon-producing embryos, while the expression level of PbWOX13a slightly increased in the later stage of somatic embryo development. Taken together, these results suggested that PbWOX13a might play a regulatory role at the later stage of somatic embryo development.

    SE is a highly efficient method for plant regeneration[52]. Overexpression of WUS, WOX2, WOX9, BBM, and SERK is an efficient way to induce SE, and application of plant growth regulators such as auxin, MeJA, ABA, and GA is another useful method[6,47,5355]. These hormones undergo crosstalk with various TFs and play a primary role in SE[20]. However, information on interactions between phytohormones and WOX genes in P. bournei is lacking. In our study, referring to the information of cis-acting elements in the promoters of PbWOXs, we evaluated that the expression profiles of PbWOXs in embryogenic calli after treatment with IAA, MeJA, and ABA.

    Auxin was first discovered to affect embryonic initiation in carrot and has been widely used to induce SE not only in angiosperms but also in gymnosperms[56]. Moreover, studies have indicated that auxin distribution is positively correlated with the accumulation of WUS, WOX2, and WOX9 transcripts[27,57,58]. In P. bournei, the expression of WUS and WOX5/7 was induced by auxin. However, the expression of WOX2 and WOX9 was inhibited, opposite to what has been reported in Picea abies[49]. In view of this phenomenon, we analyzed the possible causes of species differences or differences in auxin concentration. Whether WOX2/WOX9 and auxin play a synergistic or antagonistic role in somatic embryo initiation remains to be determined.

    ABA involvement in embryo development and maturation has been demonstrated in the SE of several species. In late embryonic development, LEA proteins accumulate in large quantities and act as components of ABA-inducible systems. On the other hand, exogenous ABA in culture media has been shown to promote the maturation and regeneration of somatic embryos[55]. Previous studies have shown that embryo cells cultured in media supplemented with 100 μM ABA produced more embryos in sugi[59]. Six SlWOXs were significantly upregulated after 3 h of 100 μM ABA treatment in tomato[60]. Our data showed that PbWOX11/12a, PbWOX11/12b and PbWOX11/12c were also briefly induced after 3 h of ABA treatment. At the same time, these three genes were highly expressed in the cotyledon-producing embryo stage of SE. It was further speculated that the expression of PbWOX11/12s is likely to be activated by ABA signaling, thereby promoting somatic embryo maturation.

    MeJA is another hormone that increases somatic embryo induction and maturation rate. The effect of MeJA is similar to that of ABA to some extent, but it cannot replace ABA[33]. Previously, 50 μM and 100 μM MeJA were used to treat embryonic calli of longan[61], and exogenous applications of 10-400 μM MeJA produced more mature somatic embryos to different extents[62] Here, we used qPCR to measure the expression changes of PbWOXs after 100 μM MeJA treatment and hoped to determine the relationship between PbWOXs and MeJA. Our data showed that the expression levels of PbWUS and PbWOX11/12a were induced rapidly after MeJA treatment. In addition, the expression levels of PbWOX2a and PbWOX9 were inhibited by MeJA after 3 h. Therefore, applying MeJA to calli for a suitably short time might promote the somatic embryo differentiation process in P. bournei.

    The WOX family is unique to plants, and WOX members play important regulatory roles in plant development, such as embryonic patterning. In the present study, we identified 15 PbWOX members in P. bournei, and their expression patterns among different tissues and SE process were determined, and the relationships between PbWOXs and hormones were also analyzed. These results are helpful to further study the regulatory roles of PbWOXs during SE, thus provides the important gene resources for regulating the SE process in P. bournei and other forestry trees.

    We acknowledge Wenting Xu from Zhejiang A&F University for providing basic experimental materials. We thank for professor Longjun Cheng (Zhejiang A&F University) for his guidance. This work was supported by the Zhejiang Science and Technology Major Program on Agricultural New Variety Breeding (2021C02070-10), the National Natural Science Foundation of China (32171828 and 32101545).

  • The authors declare that they have no conflict of interest.

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  • Cite this article

    J Pérez-Moreno, PE Mortimer, J Xu, SC Karunarathna, H Li. 2021. Global perspectives on the ecological, cultural and socioeconomic relevance of wild edible fungi. Studies in Fungi 6(1):408−424 doi: 10.5943/sif/6/1/31
    J Pérez-Moreno, PE Mortimer, J Xu, SC Karunarathna, H Li. 2021. Global perspectives on the ecological, cultural and socioeconomic relevance of wild edible fungi. Studies in Fungi 6(1):408−424 doi: 10.5943/sif/6/1/31

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Global perspectives on the ecological, cultural and socioeconomic relevance of wild edible fungi

Studies in Fungi  6 Article number: 31  (2021)  |  Cite this article

Abstract: Wild edible fungi (WEF), including mushrooms and truffles, comprise a natural source of nutritious and healthy food. The consumption of WEF began at least 18, 700 years ago during the Stone Age. Current data from over 100 countries indicates the existence of more than 2, 100 edible species, a figure that is continually growing, as vast regions and many cultures remain understudied. However, only around 30 species of WEF are grown commercially at a large-scale. WEF also play a key ecological role in the structure and functioning of natural ecosystems and have significantly contributed in shaping all life on the planet. Either as food, medicine or both, they are important for the survival, cultures, and economies of hundreds of ethnic groups around the globe. Over the last 15 years, there has been a noteworthy increase in the international trade of WEF, which is currently estimated at billions (USD) annually. In 2017, the WEF global trade, of either fresh or processed products, exceeded 1, 230, 000 tonnes. Due to their ecological, sociocultural and economic importance, the international WEF trade has a role to play in the postpandemic recovery period. The main challenge of this period will be maintaining natural ecosystems while simultaneously improving human wellbeing. Critical elements of this challenge include ensuring food security, enhancing rural development, creating sustainable jobs, mitigating hunger, and slowing the loss of traditional knowledge generated over millennia. This review analyzes the ways in which sustainable use of WEF could contribute to achieving these goals.

  • Wild edible fungi (WEF) have been consumed by humans for thousands of years. The earliest evidence of consumption dates back to the Upper Paleolithic period around 18, 700 years ago (Power et al. 2015). They have also played a paramount role in the structure and functioning of natural ecosystems across the planet. As saprotrophs, mycorrhizal symbionts, or parasites, WEF have contributed in shaping all life on the planet. Since the Carboniferous period, saprotrophic mushrooms, mainly those belonging to Basidiomycetes, have played a vital role in nutrient cycling, primarily through digesting lignocellulosic materials previously resistant to decomposition. Ectomycorrhizal mushrooms function as a type of communication network in the forests by establishing connections among plants through which nutrients, water and signal molecules are exchanged. Parasitic mushrooms regulate plant community structures in ecosystems. It has even been shown that mushroom spores (including those of WEF), the production of which is estimated to be around 50 million tonnes annually, can stimulate rainfall (Hassett et al. 2015). A metanalysis of the diversity of WEF around the world revealed that approximately half of global diversity is concentrated across only eight families: Agaricaceae, Amanitaceae, Boletaceae, Cantharellaceae, Cortinariaceae, Gomphaceae, Russulaceae and Tricholomataceae (Fig. 1). Six of these families contain typical ectomycorrhizal species, showing the enormous dominance of this ecological group. In contrast, in China and Mexico, the two main biocultural repositories of WEF in the world, just five fungal families comprise around half of all WEF species consumed: Agaricaceae, Boletaceae, Gomphaceae, Russulaceae and Tricholomataceae (Fig. 2A, B, respectively).

    Figure 1.  Distribution of families of 2, 100 species of wild edible fungi reported worldwide. Based on data from Boa (2004), Wu et al. (2019) and Pérez-Moreno et al. (2020d)

    Figure 2.  Distribution of families of WEF in the two main biocultural repositories of WEF in the world: 1, 020 species of WEF reported from China among 55 ethnic groups (a) and 450 species from Mexico among 68 ethnic groups (b). Based on data from Wu et al. (2019) and Pérez-Moreno et al. (2020d), respectively.

    From an anthropocentric perspective, WEF and their multitudinous uses constitute an enormously important component of the traditional livelihood systems of numerous ancient cultures around the world (Pérez-Moreno et al. 2020a). It has been demonstrated that WEF are not only a nutritious food source, but that they also enhance the immune system and contain bioactive compounds with anticarcinogenic, antihypertensive, antioxidant, antibiotic and antiviral properties (Pérez-Moreno & Martinez-Reyes 2014). Therefore, the consumption of WEF constitutes not only a form of sustenance and economic activity for impoverished communities, but also a natural treatment for illnesses. The annual international trade of WEF has been estimated at 1.2 billion tonnes, with a 3-fold increase in the last two decades alone (de Frutos 2020). This trade has been estimated to be worth more than USD 5 billion. However, the use of WEF presently faces enormous challenges, including high rates of deforestation, biodiversity loss, rapid cultural erosion, unfair trade and climate change.

    Fortunately, a promising future for WEF might yet be possible by implementing sustainable strategies such as adopting fair trade practices, successful reforestation efforts, application of innovations including mycotourism, sustainable harvesting techniques and widespread cultivation of mushrooms. Additionally, due to the fact that most edible mushrooms are quickly perishable, a suitable alternative is the technology transfer, to producers or gatherers, of methods to extend the WEF shelf life and at the same time to provide increasing revenues by providing and added value. These methods include for example drying, canning, preservation in vinegar or brine and production of jams, mushroom soup powder or bakery products. Successful commercialization of these added value products requires a quality control which should include information related to its nutritional data, date of packaging and due date. These strategies meet 11 out of the 17 Sustainable Development Goals of the United Nations Agenda for 2030 and have therefore attracted international interest (UN 2020). Accordingly, we present a review on the global ecological, sociocultural and economic relevance of WEF and analyze the challenges and perspectives towards WEF in the post-pandemic period.

  • The structural and functional diversity of WEF (Fig. 3) has played a crucial role in the development of life on the planet. Fungi are heterotrophic organisms, which mean that they are unable to generate their own food. For this reason, they have evolved to develop three trophic mechanisms. The first group are saprotrophic species, which feed on dead organic material of plants, animals or other organisms. The global ecological function of these fungi is essential for nutrient recycling in both natural and man-made ecosystems. Of particular importance are the Basidiomycetes fungi to which most WEF belong. Among the 2, 180 species of WEF reported worldwide by Li et al. (2021), 92.29% (2, 012 species) are Basidiomycetes, and the remaining 7.71% (168 species) are Ascomycetes (Fig. 4a). During the Carboniferous period 300 MYA ago, life on the planet as a whole was in a precarious state, largely because of the accumulation of plant debris, comprised mostly of cellulose and lignin. No organisms that were capable of degrading these compounds existed at the time, threatening a number of ecosystems across vast stretches of the planet. A mutation enabled an early lineage of Basidiomycetes fungi to produce enzymes belonging to the peroxidase family, which were able to degrade lignocellulosic compounds and recycle plant debris. As a consequence of this process, global ecosystem functioning was able to continue (Floudas et al. 2012). At the same time, the ancestors of Basidiomycetes experienced enormous structural and functional diversification that is still appreciable today. Basidiomycetous fungi are still excellent lignin decomposers in nature, demonstrating an "evolutionary footprint" which can be defined as a current characteristic present in living being's consequence of ancient genetic adaptations (Nagy et al. 2016, Ayuso-Fernandez et al. 2018).

    Figure 3.  Examples of the diverse range of morphological traits in wild edible fungi. A Amanita basii from pine forests in Central Mexico. B Auricularia auricula-judae from a cloudy subtropical forest in Machu Pichu, Peru. C Boletus reticuloceps in an Abies forest in China. D Terfezia arenaria from a sandy grassland in Morocco. E Tuber indicum from pine forest in Sichuan, China. F Cantharellus cibarius from a mixed broadleaf woodland in Scotland, United Kingdom.

    Figure 4.  a Trophic groups (in percentages) of the 2, 180 known wild edible fungi. b the main cultivated saprophytic mushroom species in the world in relation as a percentage of the total global production (34 billion kg). Percentages were estimated from data presented by Li et al. (2021) and Royse et al. (2017).

    A great variety of edible saprophytic fungi of enormous sociocultural and economic importance belong to Basidiomycetes, including numerous species belonging to the genera Auricularia, Agaricus, Flammulina, Lentinula, Pleurotus and Volvariella. However, there is also a small proportion of parasitic fungi that can be classified as WEF, such as members of Armillaria, Desarmillaria, Laetiporus and Ustilago. Parasitic fungi take their nutritional sources from plants, animals and microorganisms (including fungi themselves), causing damage, disease, death or simply living at the expense of the host organism. Paradoxically, epidemiological studies have shown that parasitic fungi regulate the structure of plant communities in natural ecosystems, maintaining biodiversity within an ecosystem by limiting the dominance of any particular species, thus fulfilling an ecological niche of enormous importance (Termorshuizen 2016).

    The third trophic group consists of mycorrhizal fungi, which enter into mutualistic relationships with plants, significantly influencing forest structure and helping to facilitate the maintenance of all life on the planet. Mycorrhizal fungi feature a mutualistic feeding mechanism, wherein fungi receive carbon compounds from the plants with which they establish a relationship and in return they transfer water and macro- and micronutrients from the soil to their host plants. This symbiotic relationship is established among the roots of approximately 5, 000 plant species, including both gymnosperms and angiosperms, which dominate boreal, temperate and some subtropical as well as tropical biomes around the planet. The mycelium of these fungi penetrates the interstitial spaces between cortical cells of the host plant roots, from where they grow outward, forming fungal mantles that cover the host plant roots profusely and then later form mycelial networks that connect trees of different ages within the forest (Beiler et al. 2010). Thus, mycorrhizal networks constitute "… a kind of below ground internet which has been termed appropriately as the wood wide web…" (Rhodes 2017), since trees can utilize these complex assemblages to exchange water, carbon, nitrogen and other nutrients and minerals, conduct signaling between individuals, and send out defense compounds and allelochemicals. Moreover, because these networks facilitate the sharing of resources between trees of different species, including between angiosperms and gymnosperms, this discovery has shown that the functional traits of trees in forest ecosystems are more complex than previously believed (Tedersoo et al. 2020). The most economically lucrative WEFs in the world belong to this trophic group, which include truffles (Tuber spp.), Chantarelles (Cantharellus spp.), Porcini (Boletus spp.), Matsutake (Tricholoma matsutake and allied species) and Caesar's mushrooms (Amanita sect. caesarea). Li et al. (2021) reported 2, 180 species of WEF, among which 1, 181, 940 and 59 belonged to ectomycorrhizal, saprophytic and parasitic trophic groups, respectively (Fig. 4a). Despite this, only a miniscule number (100 species) are commercially cultivated, and only 10 of these are produced globally on an industrial scale: Auricularia auricula-judae, A. nigricans, Agaricus bisporus, Flammulina velutipes, Lentinula edodes, Pleurotus cornucopiae, P. eryngii, P. nebrodensis, P. ostreatus and Volvariella volvacea (Reis et al. 2012, Royse et al. 2017) (Fig. 4b).

    Additionally, recent discoveries have revealed the enormous functional importance of wild fungi spores in their maintenance of local micro-climates by inducing rainfall. This includes WEF such as Lactarius hygrophoroides, Russula aeruginea, R. pulchra, R. variata and Suillus brevipes. The annual production of airborne fungal spores has been estimated to be around 50 million tonnes. It has been shown that due to their dispersal mechanisms, stimulated by the secretion of mannitol and other hygroscopic sugars, these spores constitute aerosols that have the potential to act as condensation nuclei for large water droplets, aiding in the formation of clouds and later in the generation of rain (Hassett et al. 2015).

  • The multitudinous uses of WEF constitute an enormously important component of subsistence livelihood systems developed over millennia. The first evidence of WEF consumption can be dated to 18, 700 years ago in the Upper Palaeolithic Period. An analysis of the dental plaque of the so-called "Red Lady" in northern Spain revealed the presence of various plant remains and fungal spores from an Agaric and a bolete (Power et al. 2015) related to Boletus edulis, a known WEF species from Europe. In other parts of the world, evidence of the consumption of WEF has also been documented: i) the Roman historian Pliny documented the consumption of wild edible mushrooms associated with oaks in his Natural History (Naturalis Historia) written between 77 and 79 AD, one of the most important encyclopaedic documents concerning ancient knowledge from the Roman Empire. In Chapter 11 of Book XVI, titled "The Natural History of the Forest Trees" he mentions: "… Such is the multiplicity of the products borne by the robur in addition to its acorns; and not only these, but mushrooms as well, of better or worse quality, the most recent stimulants that have been discovered for the appetite; these last are found growing about its roots. Those of the quercus are the most highly esteemed, while those of the robur, the cypress, and the pine are injurious…" (Bostock & Riley 1855). Furthermore, during the Song Dynasty in China from 960 to 1127 AD, Wu San Kwung discovered that by slashing the bark of forest logs where Lentinula edodes (shiitake) was naturally growing and vigorously hitting them, it was possible to increase the natural production of this mushroom. Due to this successful discovery, he is considered the father of shiitake cultivation. Even older documents record its use in ancient China, where it was called "ko-ko" or "hoang-mo" (Wasser 2005). Finally, the first known palaeographic evidence of WEF consumption in the Americas can be found in The Florentine Codex. This ancient book was written in Spanish and Nahuatl in Mexico between 1540 and 1577 by the friar Bernardino de Sahagún. Informed by traditional Aztec cultural practices, it contains a whole section in Chapter VII titled "Second paragraph: Of the mushrooms" (Parrapho Segundo: de las setas) that is dedicated to the WEF consumed in Mesoamerica, including those WEF with ceremonial uses (Fig. 5). This work reveals the wealth of WEF knowledge maintained generationally and transmitted by locals before the arrival of the conquistadors, including the common names of the WEF, cooking methods, and morphological and ecological characters of a number of species (Sahagún 2019). In a number of ancient cultures that are still living, there survives an incredible linguistic diversity used to describe WEF, which is evidence of prolific WEF knowledge widely disseminated across the five continents; for example, in Mexico, over 5500 native names are used to designate different kinds of WEF (Pérez-Moreno et al. 2020b).

    Figure 5.  The first paleographic evidence of wild edible mushroom consumption in the Americas can be found in the Florentine Codex (with pictures), written between 1540 and 1577 in Central Mexico by Aztec men and the friar Bernardino de Sahagún, currently held in the Laurentian Library of Florence, Italy.

    Boa (2004) recorded over 2, 100 edible species of mushrooms and truffles across 85 countries. More recently, Li et al. (2021) identified 2, 189 edible species from 99 countries, among which 2, 006 can be consumed safely, and 183 species require a pre-treatment prior to safe consumption or are associated with allergic reactions by some people. Two of the most important biocultural centres in the world, where traditional knowledge that was generated over millennia still survives today, are China and Mexico. China has 1, 020 species of WEF (Wu et al. 2019) and 56 ethnic groups (55 of which are minority groups, with the Han people comprising the majority group); and Mexico has more than 450 species of WEF, 300 of which are commercialised, and 68 ethnic groups (Pérez-Moreno et al. 2020b, d). These ethnic groups are understudied, but recent surveys have shown them to be characterized by deep mycophilia. For example, in Mexico, only approximately 500 Tlahuica-Pjiekakjoo people are alive today, all of whom are over 60 years old. Members of this ethnic group, however, are capable of distinguishing more than 160 species of WEF (Pérez-Moreno et al. 2020b). In addition to this, there are important groups such as the Mixtec people (the third largest native group in Mexico, only after the Nahuatl and Maya groups) (Hernández-Santiago et al. 2016) or the Chinantec people (López-García et al. 2020), whose cultures have only recently been examined through an ethnomycological lens. Meanwhile, in Europe there are 87 distinct indigenous peoples, of which 33 form the ethnic majority population in at least one sovereign state, while the remaining 54 constitute ethnic minorities (Pan & Pfeil 2002). However, compared to Mexico, most European countries consume a relatively much smaller species number of WEF, e.gr. across 24 countries in Europe, the number of commercialized WEF species is as low as 268 (Peintner et al. 2014). Regions of Western Europe, however, such as the Mazovia region in Poland, where 72 species of WEF are consumed, feature extensive mycophilia as central parts of their cultures and economies (Kotowski et al. 2019). However, as mentioned above the largest centre of diversity of WEF with 1, 020 species (Wu et al. 2019), and 55 minority ethnic groups, is China. For example, very recently Zhang et al. (2021) collected and analysed 3, 585 samples of WEF from markets located in 35 counties across Yunnan Province and identified 159 WEF species. This is a representative example of the large diversity of WEF currently consumed in some Chinese areas, which should then be considered global hotspots. Recently, the opportunity to commercialize new WEF species in local markets dominated by ethnic groups such as the Yi people in southwest China has also gained attention (e.g., Wu et al. 2016, Wang et al. 2020).

    Additionally, mycophilia is common in other countries around the world. In Europe, countries that have some mycophilic traditions include Finland, France, Italy, Spain, Sweden and Ukraine, as do Cameroon, Tanzania, Zimbabwe and Morocco in Africa, China, Japan, Russia and Mongolia in Asia, Mexico and Guatemala, with a growing interest in the USA and Canada, in North America, and finally New Zealand and Australia in Australasia (Pérez-Moreno et al. 2020a). Although the diametrically opposing concepts of mycophilia and mycophobia can be helpful to generalize viewpoints regarding WEF, we should be cautious about overutilizing this dualistic framework and understand that general attitudes toward mushrooms can be nuanced and change over time.

    In general terms, there are three patterns of WEF consumption and trade in the world: i) self-consumption; ii) commercialization in domestic markets; and iii) commercialization in international markets. Each of these patterns faces its own challenges, weaknesses, and potential benefits. The most basic and oldest form of WEF consumption that can be widely found throughout the world is self-consumption. This category of consumption has been an important part of the subsistence and culture of low-income groups in Mesoamerica, Asia and Africa and continues to be an important part of the survival of millions of people in many cultures. Hundreds of WEF species are collected and consumed in these areas annually during their respective rainy seasons, and they constitute a fundamental element in the diet of numerous ethnic groups. Nutritionally, various studies have documented that, in general terms, WEF are an important source of protein, vitamins and minerals, and are low in fat, carbohydrates, cholesterol and triglyceride contents (Hall et al. 2003). Additionally, it has been documented that WEF species are an important source of bioactive compounds with medicinal properties, including compounds with anticarcinogenic, antidiabetic, antihypertensive, antioxidant, antimicrobial, antibacterial and antiviral properties as well as immune system enhancers (Pérez-Moreno & Martínez-Reyes 2014). For example, of the edible species consumed in China and Mexico, 30% and 15% have medicinal properties, respectively (Bautista-González & Moreno-Fuentes 2014, Wu et al. 2019). Of the WEF produced for self-consumption, some species that have a short shelf life or are produced in small quantities, such as members of the Suillus or Hygrophorus genera, are consumed by low-income groups where the value as a food is higher compared to that generated by their commercialization outside their communities. Additionally, species such as Neolentinus lepideus, which is the first WEF that appears during Mexico's mushroom season and has great biocultural importance for the Zapotec ethnic group, are not commercialized due to their high cultural and culinary value. In the last few decades, developed countries in North America and Europe have been increasingly organizing mycological field trips and forays in their local forests to collect species and later consume them. In the latter case, species that are either easily recognized based on their morphoanatomical characteristics or are comparatively abundant are usually collected and consumed, such as chanterelles (Cantharellus cibarius s.l.), boletes (Boletus edulis s.l.), morels (Morchellas pp.), "chicken of the woods" (Laetiporus sulphureus) and "Caesar's mushroom" (Amanita sect. caesarea). Currently, there is also a large and growing number of mycological fairs around the world, with a wide range of goals, including selling fresh and/or processed mushrooms, educating the public on how to distinguish between edible and toxic species, biocultural revaluation, conferences by specialists, mushroom identification workshops, commercialization of mushroom handicrafts, and the sale of artistic products created by local people.

    Regulations have been established for the collection of WEF, whether for personal or commercial use, in various countries such as Austria, Argentina, Belarus, Bosnia and Herzegovina, Canada, Chile, Croatia, Finland, France, Italy, Macedonia, Montenegro, Poland, Rumania, Russia, Serbia, Spain, Slovakia, Spain, Sweden, Switzerland and USA (e.g., De Michelis & Rajchenberg 2006, Martínez-Peña et al. 2011, Peintnerpan2006bpeintner et al. 2013, BCG 2020, PFNMBN 2020, Wild Food UK 2020, VMS 2020). Regulations vary on a country-by-country basis, but in general they tend to limit which species are allowed for collection, the quantity allowed for collection (for personal or commercial consumption), and the frequency of collections in public areas (private areas or ecological reserves usually either require special permits or collection is outright forbidden). In addition, there are specific recommendations for sustainable harvesting of WEF, defined as the rate of extraction being equal to or less than the rate of production. Certain regulations designed to increase sustainable harvests include those meant to encourage collecting mushrooms using a knife and basket to promote the dissemination of spores in the gathering areas, cutting the mushroom stem above the ground in order to avoid damaging the mycelial masses, not collecting mushroom primordia, never picking more than half of the mushrooms that you find, or staying away from places of scientific interest, such as rare ecosystems.

    Traditional knowledge of and culinary traditions associated with WEF constitutes an important part of the worldview of indigenous people, and is a valuable component of world cultural heritage (Fig. 6). Additionally, the collection and consumption processes of WEF have been used to strengthen social relationships in ethnic groups. This process begins with the gathering process, since it requires members of different generations to spend long periods of time together. It continues when members of the communities with more knowledge transmit their valuable expertise to younger generations, oftentimes communicating in their native languages. This is how traditional knowledge and its attendant vocabulary has been maintained across millennia in cultures around the world, and it continues even now in low income groups. After the collection stage, there are cultures that still use surplus gathered WEF as gifts to friends or family members of the community, or as barter for other foods or goods, further strengthening cultural ties. Finally, during the process of preparing food dishes, there is a sort of revalidation of cultural identity, since there is an enormous diversity of dishes that use local ingredients, and that constitute part of the myco-gastronomical characteristics of each of the different regions of the world where WEF are consumed. In fact, the astonishing diversity of local gastronomy is considered part of the biocultural heritage of humankind, and as such should not only be preserved, but also promoted as a strategy to maintain food security through the diversification of food sources. These perspectives and their global relationships to food security, biocultural conservation and forest sustainability have been recently reviewed in detail by Pérez-Moreno et al. (2021).

    Figure 6.  Sociocultural diversity of edible wild mushrooms in different cultures. A Nahua gatherer selling a diversity of mushrooms in Central Mexico. B Lyophyllum decastes marketing by Nahua women in Texcoco, Mexico. C Tricholoma matsutake sale in Ciba Market, Kunming, China. D Ramaria araiospora being sold by Otomi people in Jilotepec, Mexico. E Yi woman holding specimens of Tuber indicum in a truffle festival in Yongren, China. F Tajin with desert truffles (Terfezia arenaria and T. claveryi) in Morocco. G Berber woman collecting desert truffles associated with Helianthemum guttatum in a sandy grassland in Morocco, northern Africa.

    WEF themselves are a genetic resource of enormous importance for global food security. There is an enormous number of species with the potential for cultivation, many of which could contribute to food self-sufficiency, creation of local jobs and poverty mitigation. In fact, the fungal germplasm of the 30 or so species of edible mushrooms cultivated globally at an industrial level were once wild mushrooms. This number dramatically contrast with the more than 2, 000 EWF which have been worldwide recorded (Li et al. 2021). However, only a small number of them (lower than 1.5%) has been industrially cultivated constituting therefore an untapped genetic pool. This despite the fact that EWF constitute a source of healthy food, which is rich in essential aminoacids, fibre, vitamins and minerals and low in cholesterol, and calories. More recently their importance as functional foods and their potential as health potentiators and elicitors of immune system has also been documented. As a consequence, rising consumption of unhealthy processed food items and increasing awareness among consumers related to the health benefits of mushrooms are important factors which are driving an increasing production of mushroom cultivation. For example, world production of cultivated edible mushrooms increased 30-fold since 1978 (from 1 billion Kg that year to 34 billion Kg in 2013). Meanwhile, world population increased only about 1.7-fold during the same period (from 4.2 billion to 7.1 billion), which represented an increase of per capita mushroom consumption, especially since 1997, accounting annually 1 kg per person that year versus 4.7 kg in 2013 (Bunyard 2021). Despite this fact, a global demand for healthy and nutritious food, including edible mushrooms continues to accelerate, and then a diversification boost of the cultivation of the known EWF genetic pool is currently an urgent need.

  • The economic importance of WEF exists on multiple levels. The most basic level is the commercialization in local communities in which the gatherers directly participate, the next level is the sale of WEF in regional markets carried out by 1–2 broker chains, followed by sale in national markets conducted by chains of up to 3 to 5 brokers. A crucial factor to consider is that in developing countries, mushroom pickers, regardless of gender, often belong to marginalized groups. Mushrooms are accordingly an important source of family income during harvest time, given the vulnerable socioeconomic status of mushroom collectors in parts of Africa, Mesoamerica and Eastern Asia. Little data exist regarding the commercialization of WEF in domestic markets around the world. However, there are some examples that are emblematic of what might exist globally. For example, in some Mexican communities, it has been documented that up to 100% of family income during the wet season comes from mushroom harvesting (Pérez-Moreno et al. 2010). In western North America, WEF collection constitutes an important source of income for immigrant groups coming from mycophilic cultures (Pilz & Molina 2002); and in China, there has been a radical change in the social position of previously marginalized groups that have traditionally collected and sold WEF such as matsutake (Arora 2008).

    At the highest level, WEF are traded internationally for billions of US dollars annually (Table 1). Some species fetch exorbitant prices, placing some WEF among the world's most expensive foods. Some examples of these are as follows: i) In 2019 one fruiting body of the European white truffle (Tuber magnatum), weighing 1.005 kg, was sold for USD 145, 000 at an auction in the "89th International Alba White Truffle Fair" in Alba, Italy (AFP 2019); ii) Japanese matsutake (Tricholoma matsutake) can be worth up to USD 2, 000 per kg, and USD 1, 000 per kg during the beginning of the season in Tokyo is a common price (Japan Info 2020); iii) Perigord black truffle (Tuber melanosporum) prices ranged from USD 2, 811 to 3, 565 per kg from November 2019 to July 2020 (Truffle farm 2020); and iv) Annual world production of chanterelles (Cantharellus cibarius s.l.) ranges from 150, 000 to 200, 000 tonnes with an estimated value of USD 1.67 billion (Watling 1997). In addition to these examples, there are a number of WEF whose international commercial value is of relevance due to their exceptionally high level of production, e.g., Porcini (Boletus edulis s.l.), Caesar's mushroom (Amanita sect. Caesarea), Morels (Morchella spp.), Saffron Milk caps (Lactarius sect. Deliciousus) and Coral Fungi (Ramaria spp.). For example, a Finnish company harvested 1, 100 tons of WEF in a year, mainly porcini, with a revenue of USD 7.4 million (Cai et al. 2011).

    Table 1.  Highly prized wild edible fungi and estimated world trade value in US dollars

    Common Name Scientific name Annual in-season retail market Wholesale price (per kilogram, grade one)
    Chanterelle Cantharellus cibarius s.l. $1.67 billion $8 to $22
    Chinese black truffle Tuber indicum $170milliona $50 to $200b
    Desert truffle Terfezia spp. and Tirmania spp. Unknownc $27 to 334
    Ganbajun Thelephora ganbajun Unknownd $50 to $250
    Italian white truffle Tuber magnatum $150 million $1, 000 to $7, 500b
    Matsutake Tricholoma matsutake s.l. $500 million $30 to $1, 000
    Périgord black truffle Tuber melanosporum $150 million $250 to $3, 200b
    Porcini Boletus edulis s.l. $250 million $13 to $198
    Updated from Pérez-Moreno & Martinez-Reyes 2014; aestimation based on an average price of USD 170 provided by Truffle farm (2020) and a production of 1, 000 tonnes (Bin et al. 2021). bBased on retail prices in 2019 in Truffle farm (2020); cmostly sold in Arab countries with no official data available; dmostly sold in domestic markets in Southwestern China, without current accurate estimations of natural production.

    International trade of WEF has increased dramatically in recent decades. According to United Nations data, the volume of WEF trade has increased more than three-fold in the last 15 years (Fig. 7). The main variables that seem to drive this growing business are dynamic changes of trade relations between developed countries, income (gross domestic product) changes in some countries, and modification of consumption habits (including the increasing desire for healthy foods and diet diversification). The countries that have shown the greatest increase in trade of WEF between 2002 and 2017 in America are Canada, Mexico and Peru; in Europe they are Belgium, Bulgaria, Latvia, Macedonia and Romania; in Africa it is Belgian Congo; in Asia they are Armenia, Azerbaijan, Bhutan, India, Kyrgyzstan and Pakistan; and in Australasia it is New Zealand (de Frutos 2020). In addition to these figures, it should be considered that the domestic trade in many countries, such as Australia, China, France, Italy, Japan, Mexico, New Zealand and Spain, has yet to be holistically evaluated and likely accounts for millions of USD annually (Fig. 8).

    Figure 7.  Annual global trade of edible wild mushrooms and truffles from 2002 to 2017. Graph created with data from the United Nations published by de Frutos (2020). "Total" includes the sum of international mushroom and truffle trade indexes labelled with the codes 070959 (truffles and mushrooms fresh or chilled), 071159 (mushrooms, provisionally preserved but unsuitable in that state for immediate consumption), 071239 (mushrooms and truffles, whole, cut sliced, broken or in powder but not further prepared, dried), and 200390 (mushrooms prepared or preserved otherwise than by vinegar or acetic acid). Meanwhile "Fresh or chilled" refers only to international trade labelled with the trade code 070959 (truffles and mushrooms fresh or chilled).

    Figure 8.  Economic relevance of edible mushrooms in different continents. A Mexican gourmet dish with the native "Blue milk cap" (Lactarius indigo). B Chinese gourmet desert with Asian truffles (Tuber indicum); C Vodka aged for 5 years with Cantharellus cibarius s.l. in Russia; D Complex factory of enoki mushrooms (Flammulina velutipes) in Nagano, Japan with an annual production of 300 thousand tonnes. E Specialized store selling Périgord black truffle (Tuber melanosporum) products in Cahors, France. F Hazel and oak tree plantation "Tewnion Truffiere" which produce high quality Périgord Black Truffles in Christchurch, New Zealand.

    Currently cultivation of edible saprotrophic mushrooms constitutes a multibillion-dollar industry, with cutting edge technological applications. For example, in Suwa, Japan, there is an industrial complex dedicated exclusively to the cultivation of enokitake mushrooms (Flammulina velutipes), where more than 300, 000 tonnes are produced per year. Amazingly, as most of the processes are automated, the factory complex is run by only 200 workers. Furthermore, a novel stream of income for rural communities might exist in the future via the large-scale trade of edible ectomycorrhizal mushrooms used to produce bioinoculants useful for forest plant production, which are critical to ensuring the success of reforestation efforts (Pérez-Moreno et al. 2020c).

  • One of the main challenges faced by humankind today is figuring out how to balance nature conservation and human livelihoods. Nature conservation priorities include the maintenance of forest masses and natural ecosystems in order to mitigate climate change, slowing and reversing the accelerated extinction rate in order to preserve biodiversity, and preparing for the possibility of new pandemics (zoonoses) in the near future. At the same time, protecting human livelihoods should include the fair distribution of financial profits for people living in impoverished conditions, the promotion of rural development, food diversification, food sustainability and job creation, and reduction of environmental pollution and hunger. A comprehensive outline of the specific challenges facing humankind is the 17 sustainable development goals set by the 2030 United Nations agenda (UN 2020). To advance the strategic development of these goals, WEF constitute a genetic, biocultural and economic resource of enormous global import. In order to contribute to these 17 goals, the following actions must be promoted: i) the diversification of the cultivation of saprobic species at an industrial scale; ii) the improvement of techniques for the cultivation of ectomycorrhizal species; iii) the development of bioinoculant technologies based on edible ectomycorrhizal fungi that are useful for successful reforestation efforts; iv) the promotion of sustainable harvesting techniques to avoid overharvesting of WEF; v) the application of innovations such as mycotourism and the use of technologies to imbue added value to WEF, particularly in rural communities; vi) the dissemination of ecological, sociocultural and economic knowledge of mycological resources to children and young people; vii) the rescue and revaluation of local mycogastronomical practices; viii) the development of gourmet mycogastronomy; and finally, ix) promotion of the fair distribution of generated profits for local communities. Achieving these objectives requires the promotion of strategic alliances between four sectors: a) rural and urban communities; b) decision makers and policy makers; c) groups of scientists; and d) entrepreneurs, either as local cooperatives, small industries or big companies. It is important to consider that in the specific case of WEF, given the enormous cultural, social, economic, environmental and geographical variation that exists at a global level, a great amount of creativity will be required to design and implement context-specific strategies so as to suit the particular needs of an individual region, while at the same time working toward common objectives. An additional factor to consider is that in the short- and medium-term, the world will experience complex financial and sociocultural consequences of the so-called "great confinement" caused by COVID-19, which is already considered the largest economic recession in history (Snooks 2020). Therefore, immediate action to apply multiple strategies at the local, regional, national and global levels is urgently needed to counteract these negative effects. Promoting the sustainable management of WEF offers a potential pathway going forward for both vulnerable groups living in extreme poverty, as well as in urban and rural populations. The potential sustainable uses of WEF are countless; at the same time, many challenges must also be overcome to develop new innovations. The degree to which we meet these challenges will be consequential for our future.

  • Our coexistence with fungi dates back nearly 20, 000 years. Indeed, WEF have left an indelible mark on the evolution of all life forms on earth. Most of the 2, 200-known species of WEF establish ectomycorrhizal symbiosis with plant roots, accounting for 54% of total fungi, with the remaining 46% either saprotrophic (43%) or parasitic (3%). Surprisingly, only a small proportion of WEF are cultivated commercially or at an industrial scale (around 4.5%). These facts suggest that developing strategies to preserve WEF genetic resources for the purposes of food security is extremely relevant. Hundreds of WEF have traditionally been important biocultural resources critical to the livelihood strategies of poor rural communities in low or middle-income countries. On a larger scale, WEF global trade is worth billions of dollars; according to the United Nations, more than 1.2 billion tonnes were commercialized in 2017 alone. Furthermore, the volume of this trade has increased more than three-fold in the last 15 years. Therefore, WEF constitute an important natural resource which, if used sustainably, can contribute to food security, creation of jobs and hunger mitigation in the post-pandemic era to come.

    • This study was funded by a grant (No. 31861143002) of NSFC-CGIAR. The first author would like to thank Dr. Faustino Hernández-Santiago and Dr. Magdalena Martínez-Reyes for his technical help to analyze the information presented in Figures 1, 2 and 4 and to the Mexican Council of Science and Technology (CONACYT) PRONACES FOP07-2021-03 Project 316198. Peter E Mortimer would like to thank the "High-End Foreign Experts" in the High-Level Talent Recruitment Plan of Yunnan Province, 2021. Samantha C. Karunarathna thanks the CAS President's International Fellowship Initiative (PIFI) young staff under the grant number: 2020FYC0002 and the National Science Foundation of China (NSFC) under the project code 31851110759.
    • Conflict of interest
    • No conflict of interest associated with this work.
Figure (8)  Table (1) References (52)
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    J Pérez-Moreno, PE Mortimer, J Xu, SC Karunarathna, H Li. 2021. Global perspectives on the ecological, cultural and socioeconomic relevance of wild edible fungi. Studies in Fungi 6(1):408−424 doi: 10.5943/sif/6/1/31
    J Pérez-Moreno, PE Mortimer, J Xu, SC Karunarathna, H Li. 2021. Global perspectives on the ecological, cultural and socioeconomic relevance of wild edible fungi. Studies in Fungi 6(1):408−424 doi: 10.5943/sif/6/1/31
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