Previous studies identified several developmental genes, including hydrophobins ( 12), defense-related proteins ( 13), fungal cell wall (FCW) modifying enzymes ( 14– 17), transcriptional regulators ( 8, 9, 18) (e.g., mating genes), and light receptors ( 19) (e.g., white collar complex). The initial follows genetically encoded programs to develop species-specific morphologies ( 9, 10), which, in the Agaricomycetes, ranges from simple crust-like forms (e.g., Phanerochaete) to the most complex toadstools (e.g., Agaricus bisporus). While the vegetative mycelium is composed of loosely arranged hyphae and shows little differentiation, the emergence of a fruiting body initial involves a reprogramming of hyphal branching patterns to form a compact, three-dimensional structure in which hyphae adhere tightly to each other. Fruiting body development is triggered by changing environmental variables (e.g., nutrient availability), and involves a transition from vegetative mycelium to a complex multicellular fruiting body initial. Nevertheless, fruiting bodies evolved complexity levels comparable to that of simple animals, with up to 30 morphologically distinguishable cell types described so far ( 10). Uniquely, complex multicellularity in fungi comprises short-lived reproductive organs, whereas, in animals and plants, it comprises the reproducing individual. Fruiting bodies shelter and protect reproductive cells and facilitate spore dispersal. 11), cell differentiation, and defense, and execute a developmental program that results in a genetically determined shape and size ( 2, 10). During fruiting body development, fungi deploy mechanisms for hypha-to-hypha adhesion, communication (e.g., via cell−cell channels ref. 7– 10), resulting in a paucity of information on the genetic underpinnings of the origins of complex multicellularity in this group ( 2). 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).įruiting body development in mushroom-forming fungi has been subject to surprisingly few studies (see, e.g., refs. 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). The mushroom-forming fungi (Agaricomycetes) comprise >21,000 species and originated 350 million years ago ( 5), approximately coinciding with the origin of tetrapods. 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. This study provides an entry point to studying mushroom development and complex multicellularity in one of the largest clades of complex eukaryotic organisms.įungi 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). 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. 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). 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). The development of fungal fruiting bodies from a hyphal thallus represents a transition from simple to complex multicellularity that is inducible under laboratory conditions. Despite being a key step toward the evolution of complex organisms, the evolutionary origins and the genetic underpinnings of complex multicellularity are incompletely known. 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. The evolution of complex multicellularity has been one of the major transitions in the history of life.
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