Transcriptomic atlas of mushroom development reveals conserved genes behind complex multicellularity in fungi

Abstract

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. complex multicellularity | evolution | fungi | comparative genomics | fruiting body development F ungi represent a diverse lineage of complex multicellular organisms with a unique evolutionary history compared with complex multicellular animals, embryophytes, florideophytes, and laminarean brown algae (1-4). Within the fungal kingdom, complex multicellularity is discussed mostly in the context of fruiting bodies, which are found in at least eight independent lineages (2), of which the Pezizomycotina (Ascomycota) and the Agaricomycetes (Basidiomycota) contain the vast majority of species. The mushroom-forming fungi (Agaricomycetes) comprise >21,000 species and originated 350 million years ago (5), approximately coinciding with the origin of tetrapods. Fruiting bodies of mushroom-forming fungi have immense importance in agriculture, ecology, and medicine; they represent an important and sustainable food source, with favorable medicinal properties (e.g., antitumor, immunomodulatory) (6). Mushroom-forming fungi share a single origin of fruiting body formation that probably dates to the most recent common ancestor of the Agaricomycetes, Dacrymycetes, and Tremellomycetes (2).Fruiting body development in mushroom-forming fungi has been subject to surprisingly few studies (see, e.g., refs. 7-10), result...

Comparative genomics reveals unique wood‐decay strategies and fruiting body development in the Schizophyllaceae

“…and expansin‐like genes (10 of 21 genes) were likewise developmentally regulated in both species. Cerato‐platanins and expansins were mostly associated with the plant cell wall before (Baccelli, ; Tovar‐Herrera et al ., ), but their dynamic expression in fruiting bodies observed here and in previous studies (Sipos et al ., ; Krizsán et al ., ) suggests potential FCW‐related roles. Several putatively FCW‐active CAZymes (Fig.…”

“…Corresponding data for the same developmental stages (Fig. c,e) from S. commune were taken from (Krizsán et al ., ). Based on global transcriptome similarity, fruiting body samples grouped together, away from vegetative mycelia (Fig.…”

“…The 1466 developmentally regulated genes identified in A. ampla is similar in magnitude to what was reported for S. commune (2000), but less than that for species with more complex fruiting bodies (e.g. 7583 and 4425 in Coprinopsis and Armillaria ; taken from (Krizsán et al ., ). Of the developmentally regulated genes, 967 showed a significant (≥4‐) fold change in the transition from vegetative mycelium to Stage 1 primordia.…”

“…These genes showed 254‐ and 855‐fold upregulation in Stage 1 primordia of both A. ampla and S. commune , respectively, and had high expression in all fruiting body tissues (> 5000 FPKM, maximum fold change within fruiting bodies 3.4–3.7), suggesting an important role of heat shock proteins during fruiting body development. In further support of this hypothesis, homologs of these genes were found to be developmentally regulated or differentially expressed also in Laccaria bicolor fruiting bodies (Martin et al ., ), Lentinula edodes (Song et al ., ) , Armillaria ostoyae, Coprinopsis cinerea, Lentinus tigrinus and Rickenella mellea (Krizsán et al ., ). Another co‐ortholog with significant upregulation in Stage 1 primordia included A1 aspartic proteases, although the expression dynamics were somewhat different in the two species.…”

“…TF genes were identified in the 31 species based on InterPro annotations. Only proteins containing domains with sequence‐specific DNA binding ability were considered as TFs (Krizsán et al ., ).…”