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The evolution of complex multicellularity has been one of the major transitions in the history of life. In contrast to simple multicellular aggregates of cells, it has evolved only in a handful of lineages, including animals, embryophytes, red and brown algae, and fungi. Despite being a key step toward the evolution of complex organisms, the evolutionary origins and the genetic underpinnings of complex multicellularity are incompletely known. The development of fungal fruiting bodies from a hyphal thallus represents a transition from simple to complex multicellularity that is inducible under laboratory conditions. We constructed a reference atlas of mushroom formation based on developmental transcriptome data of six species and comparisons of >200 whole genomes, to elucidate the core genetic program of complex multicellularity and fruiting body development in mushroom-forming fungi (Agaricomycetes). Nearly 300 conserved gene families and >70 functional groups contained developmentally regulated genes from five to six species, covering functions related to fungal cell wall remodeling, targeted protein degradation, signal transduction, adhesion, and small secreted proteins (including effector-like orphan genes). Several of these families, including F-box proteins, expansin-like proteins, protein kinases, and transcription factors, showed expansions in Agaricomycetes, many of which convergently expanded in multicellular plants and/or animals too, reflecting convergent solutions to genetic hurdles imposed by complex multicellularity among independently evolved lineages. This study provides an entry point to studying mushroom development and complex multicellularity in one of the largest clades of complex eukaryotic organisms.

Pleurotus ostreatus is the second most cultivated edible mushroom worldwide after Agaricus bisporus. It has economic and ecological values and medicinal properties. Mushroom culture has moved toward diversification with the production of other mushrooms. Edible mushrooms are able to colonize and degrade a large variety of lignocellulosic substrates and other wastes which are produced primarily through the activities of the agricultural, forest, and food-processing industries. Particularly, P. ostreatus requires a shorter growth time in comparison to other edible mushrooms. The substrate used for their cultivation does not require sterilization, only pasteurization, which is less expensive. Growing oyster mushrooms convert a high percentage of the substrate to fruiting bodies, increasing profitability. P. ostreatus demands few environmental controls, and their fruiting bodies are not often attacked by diseases and pests, and they can be cultivated in a simple and cheap way. All this makes P. ostreatus cultivation an excellent alternative for production of mushrooms when compared to other mushrooms.

A large amount of agro-industrial waste is produced worldwide in various agricultural sectors and by different food industries. The disposal and burning of this waste have created major global environmental problems. Agro-industrial waste mainly consists of cellulose, hemicellulose and lignin, all of which are collectively defined as lignocellulosic materials. This waste can serve as a suitable substrate in the solid-state fermentation process involving mushrooms. Mushrooms degrade lignocellulosic substrates through lignocellulosic enzyme production and utilize the degraded products to produce their fruiting bodies. Therefore, mushroom cultivation can be considered a prominent biotechnological process for the reduction and valorization of agro-industrial waste. Such waste is generated as a result of the eco-friendly conversion of low-value by-products into new resources that can be used to produce value-added products. Here, we have produced a brief review of the current findings through an overview of recently published literature. This overview has focused on the use of agro-industrial waste as a growth substrate for mushroom cultivation and lignocellulolytic enzyme production.

Light is an essential factor for pigment formation and fruit body development in Cordyceps militaris , a well-known edible and medicinal fungus. Cmwc-1 , a homolog of the blue-light receptor gene white collar-1 ( wc-1 ) in Neurospora crassa , was cloned from the C. militaris genome in our previous study. Here, Cmwc-1 gene inactivation results in thicker aerial hyphae, disordered fruit body development, a significant reduction in conidial formation, and carotenoid and cordycepin production. These characteristics were restored when the Δ Cmwc - 1 strains were hybridized with wild-type strains of the opposite mating type. A genome-wide expression analysis revealed that there were 1042 light-responsive genes in the wild-type strain and only 458 in the Δ Cmwc - 1 strain. Among five putative photoreceptors identified, Vivid, cryptochrome-1, and cyclobutane pyrimidine dimer photolyase are strongly induced by light in a Cmwc-1 -dependent manner, while phytochrome and cryptochrome-2 were not induced. The transcription factors involved in the fungal light reaction were mainly of the Zn 2 Cys 6 type. CmWC-1 regulates adenylosuccinate synthase, an important enzyme for adenosine de novo synthesis, which could explain the reduction in cordycepin production. Some G protein-coupled receptors that control fungal fruit body formation and the sexual cycle were regulated by CmWC-1, and the cAMP pathway involved in light signal transduction in N. crassa was not critical for the photoreaction in the fungus here. A transcriptional analysis indicated that steroid biosynthesis was more active in the Δ Cmwc-1 strain, suggesting that CmWC-1 might switch the vegetative growth state to primordia differentiation by suppressing the expression of related genes.

Agaricomycetes are fruiting body‐forming fungi that produce some of the most efficient enzyme systems to degrade wood. Despite decades‐long interest in their biology, the evolution and functional diversity of both wood‐decay and fruiting body formation are incompletely known. We performed comparative genomic and transcriptomic analyses of wood‐decay and fruiting body development in Auriculariopsis ampla and Schizophyllum commune (Schizophyllaceae), species with secondarily simplified morphologies, an enigmatic wood‐decay strategy and weak pathogenicity to woody plants. The plant cell wall‐degrading enzyme repertoires of Schizophyllaceae are transitional between those of white rot species and less efficient wood‐degraders such as brown rot or mycorrhizal fungi. Rich repertoires of suberinase and tannase genes were found in both species, with tannases restricted to Agaricomycetes that preferentially colonize bark‐covered wood, suggesting potential complementation of their weaker wood‐decaying abilities and adaptations to wood colonization through the bark. Fruiting body transcriptomes revealed a high rate of divergence in developmental gene expression, but also several genes with conserved expression patterns, including novel transcription factors and small‐secreted proteins, some of the latter which might represent fruiting body effectors. Taken together, our analyses highlighted novel aspects of wood‐decay and fruiting body development in an important family of mushroom‐forming fungi.

With ∼36,000 described species, Agaricomycetes are among the most successful groups of Fungi. Agaricomycetes display great diversity in fruiting body forms and nutritional modes. Most have pileate-stipitate fruiting bodies (with a cap and stalk), but the group also contains crust-like resupinate fungi, polypores, coral fungi, and gasteroid forms (e.g., puffballs and stinkhorns). Some Agaricomycetes enter into ectomycorrhizal symbioses with plants, while others are decayers (saprotrophs) or pathogens. We constructed a megaphylogeny of 8,400 species and used it to test the following five hypotheses regarding the evolution of morphological and ecological traits in Agaricomycetes and their impact on diversification: 1) resupinate forms are plesiomorphic, 2) pileate-stipitate forms promote diversification, 3) the evolution of gasteroid forms is irreversible, 4) the ectomycorrhizal (ECM) symbiosis promotes diversification, and 5) the evolution of ECM symbiosis is irreversible. The ancestor of Agaricomycetes was a saprotroph with a resupinate fruiting body. There have been 462 transitions in the examined morphologies, including 123 origins of gasteroid forms. Reversals of gasteroid forms are highly unlikely but cannot be rejected. Pileate-stipitate forms are correlated with elevated diversification rates, suggesting that this morphological trait is a key to the success of Agaricomycetes. ECM symbioses have evolved 36 times in Agaricomycetes, with several transformations to parasitism. Across the entire 8,400-species phylogeny, diversification rates of ectomycorrhizal lineages are no greater than those of saprotrophic lineages. However, some ECM lineages have elevated diversification rates compared to their non-ECMsister clades, suggesting that the evolution of symbioses may act as a key innovation at local phylogenetic scales.

Fruiting bodies are among the most complex multicellular structures formed by fungi, and the molecular mechanisms that regulate their development are far from understood. However, studies with a number of fungal model organisms have started to shed light on this developmental process. One of these model organisms is Sordaria macrospora, a filamentous ascomycete from the order Sordariales. This fungus has been a genetic model organism since the 1950s, but its career as a model organism for molecular genetics really took off in the 1990s, when the establishment of a transformation protocol, a mutant collection, and an indexed cosmid library provided the methods and resources to start revealing the molecular mechanisms of fruiting body development. In the 2000s, “omics” methods were added to the S. macrospora tool box, and by 2020, 58 developmental genes have been identified in this fungus. This review gives a brief overview of major method developments for S. macrospora, and then focuses on recent results characterizing different processes involved in regulating development including several regulatory protein complexes, autophagy, transcriptional and chromatin regulation, and RNA editing.Key points•Sordaria macrospora is a model system for analyzing fungal fruiting body development.•More than 100 developmental mutants are available for S. macrospora.•More than 50 developmental genes have been characterized in S. macrospora.

Abstract Light, particularly blue light, is a key environmental factor that induces fruiting in certain agaricomycetes. In this study, we characterized mutant strains of Pleurotus ostreatus with disrupted wc-2, which encodes one of the white-collar proteins, Wc-2, to investigate the role of light in fruiting in P. ostreatus. We introduced two different plasmids containing expression cassettes for Cas9 and two different gRNAs targeting wc-2 separately into the dikaryotic P. ostreatus strain PC9×#64. Among the 11 dikaryotic hygromycin-resistant transformants, six strains did not form fruiting bodies. Genomic PCR followed by sequencing analysis suggested that all six fruitless strains were dikaryotic wc-2 disruptants. Small aggregate structures were not observed in the dikaryotic wc-2 disruptants grown under light conditions, as in PC9×#64 grown in a red box. These results suggest that Wc-2 is essential for the initiation of blue light-induced fruiting in P. ostreatus. Pleurotus ostreatus wc-2 disruptants were obtained using CRISPR/Cas9 and they were fruitingless.

• Aroma variability in truffles has been attributed to maturation (Tuber borchii), linked to environmental factors (Tuber magnatum), but the involvement of genetic factors has been ignored. We investigated aroma variability in Tuber uncinatum, a species with wide distribution. Our aim was to assess aroma variability at different spatial scales (i.e. trees, countries) and to quantify how aroma was affected by genotype, fruiting body maturity, and geographical origin. • A volatile fingerprinting method was used to analyze the aroma of 223 T. uncinatum fruiting bodies from seven European countries. Maturity was estimated from spore melanization. Genotypic fingerprinting was performed by amplified fragment length polymorphism (AFLP). • Discriminant analysis revealed that, regardless of the geographical origin of the truffles, most of the aroma variability was caused by eight‐carbon‐containing volatiles (C8‐VOCs). In an orchard of T. uncinatum, truffles producing different concentrations of C8‐VOCs clustered around distinct host trees. This clustering was not associated with maturity, but was associated with fungal genotype. • These results indicate that the variation in C8‐VOCs in truffles is most likely under genetic control. They exemplify that understanding the factors behind aroma variability requires a holistic approach. Furthermore, they also raise new questions regarding the ecological role of 1‐octen‐3‐ol in truffles.

Spent mushroom substrate (SMS) of Pleurotus ostreatus was supplemented with wheat bran and soybean flour in various proportions to obtain C/N ratios of 10, 20, and 30, and their effect was evaluated in successive cultivation of Pleurotus ostreatus , Pleurotus pulmonarius , Ganoderma adspersum , Ganoderma resinaceum , and Lentinula edodes strains with respect to mycelium growth rate, biomass concentration, recovery of the enzyme laccase and crude exopolysaccharides, and also with additional fruiting body production. All fungi showed the highest growth rate on unamended SMS (C/N 30), with G. resinaceum being the fastest colonizer (Kr = 9.84 mm day −1 ), while biomass concentration maximized at C/N 10. Moreover, supplementation affected positively laccase activity, with P. pulmonarius furnishing the highest value (44,363.22 U g −1 ) at C/N 20. On the contrary, L. edodes growth, fruiting, and laccase secretion were not favored by SMS supplementation. Fruiting body formation was promoted at C/N 30 for Ganoderma and at C/N 20 for Pleurotus species. Exopolysaccharide production of further studied Pleurotus strains was favored at a C/N 20 ratio, at the initial stage of SMS colonization. The obtained results support the potential effective utilization of supplemented SMS for laccase production from Ganoderma spp. and for new fruiting body production of Pleurotus spp.