The genetic background and transcriptome level changes during fruiting body development of fungi

Fruiting bodies are complex, three-dimensional reproductive structures, which emerged independently in many distantly related groups of Fungi. The roles of several regulators and structural genes in fruiting body development have been uncovered; yet, the general principles of fruiting body formation remain largely unknown. We set out to identified the conserved gene set underlying fruiting body initiation and development of altogether six species (Armillaria ostoyae C18, Coprinopsis cinerea AmutBmut, Lentinus tigrinus RLG-9953-Sp, Phanerochaete chrysosporium RP-8, Rickenella mellea SZMC22713, Schizophyllum commune H4-8) of distantly related groups of Agaricomycetes using comparative transcriptomics and genomics. We performed paired-end RNA sequencing on five developmental stages (vegetative mycelium, early and late primordium, young and mature fruiting body) and three tissue types (cap, lamellae, stipe). Our results demonstrate that 10-40% of the expressed genes of each species are developmentally regulated, most of which showed differential expression during fruiting body initiation. We identified numerous genes that were shared among species and showed upregulation at the early primordium stage. The molecular functions of the encoded proteins were associated with cell wall component synthesis, mRNA stability, cell growth and regulation of transcription. In addition to shared gene families, similarity was observed at the global transcriptome level, as inferred by Pearson correlation coefficients across each pairs of transcriptomes. In general, transcriptomes showed highest similarity within species, suggesting that phylogenetic affinity predicts gene expression patterns better than tissue or stage identity. Nevertheless, shared expression patterns across primordium stages of different species suggest a conserved early developmental program conserved across the Polyporales and Agaricales. This pattern was more pronounced in expression patterns of transcription factor genes, suggesting that regulators constitute a major part of this conserved developmental program. Our results contribute to understanding the general principles of fungal fruiting body development and its initiation, and represent a step towards identifying conserved and species-specific elements of fruiting body development.