Transcriptomic atlas of mushroom development highlights an independent origin of complex multicellularity

Abstract

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 (FCW) remodeling, targeted protein degradation, signal transduction, adhesion and small secreted proteins (including effector-like orphan genes). Several of these families, including F-box proteins, protein kinases and cadherin-like proteins, showed massive expansions in Agaricomycetes, with many convergently expanded in multicellular plants and/or animals too, reflecting broad genetic convergence among independently evolved complex multicellular lineages. This study provides a novel entry point to studying mushroom development and complex multicellularity in one of the largest clades of complex eukaryotic organisms.

Comparative genomics reveals the origin of fungal hyphae and multicellularity

“…We therefore, examined Ser/Thr kinase (954 clusters), hybrid histidine kinase (96 clusters), receptor (183 clusters) and adhesion (23 clusters) genes, focusing on the comparison of unicellular and filamentous fungi. Copy numbers across the 954 identified Ser/Thr kinase clusters were similar in unicellular and simple multicellular fungi, with higher kinase diversity found in complex multicellular Basidiomycota (as reported by Krizsan 2018) 86 and in Rhizophagus irregularis (Fig. 5a).…”

Unmatched level of molecular convergence among deeply divergent complex multicellular fungi

“…S1), corresponding to 19.8–66.3% of the proteome. The identified developmentally regulated genes contained 26.9-97.6%, 4.6-69.2% and 92.7% of known developmental genes of Neurospora, Aspergillus and Coprinopsis, respectively (Note S1, table S2), consistent with previous studies of fruiting body development ( 23, 28 – 30, 40 ). In a broader dataset of 19 species (see Methods) developmentally regulated genes fell into 21,267 families, of which we focused on that ones that showed conserved developmental regulation in the majority of species (Fig.…”

“…Although they originated independently, CM fungal clades are phylogenetically close, providing a tractable system for studying the genetics of major evolutionary transitions in complexity. Fruiting bodies in fungal lineages can be developmentally and morphologically highly distinct—yet they evolved for the same general purpose: to enclose sexual reproductive structures in a protective environment and facilitate spore dispersal ( 23, 27 – 30 ). Here we seek to explain the convergent evolution of fungal fruiting bodies by analyzing the fate of multicellularity-related gene families across the two largest clades of CM fungi: the Agaricomycotina (mushroom-forming fungi, Basidiomycota) and the Pezizomycotina (Ascomycota).…”

High-throughput targeted gene deletion in the model mushroom Schizophyllum commune using pre-assembled Cas9 ribonucleoproteins

“…In addition to gene deletion, these techniques can be modified to produce other genome edits, including promoter replacement and targeted gene integration (knock-in). Recent efforts in genome and transcriptome sequencing of mushroom-forming species have resulted in a large number of candidate gene families involved in mushroom development and other processes 11,14,41,42 . The important addition of Cas9 RNP-mediated genome editing to the molecular toolkit of S. commune will facilitate the functional characterization of these gene families, leading to important new insights into the biology of this important group of fungi.…”