Understanding the genomic and transcriptomic changes leading to morphological simplification in fruiting body forming Basidiomycete Schizophyllum commune

The evolution of complex multicellular development is affected by a range of genetic innovations, among which changes to the regulatory repertoire are generally considered to have great significance. Throughout evolution we can observe a definite tendency of morphological complexity being coupled with the size of the gene regulatory apparatus – mainly with the number of transcription factors (TFs). Our study focuses on placing morphologically simplified organisms in this chart: do we see a decreased number of TFs in simplified organisms compared to their more complex relatives? In order to find out we performed comparative genomic analysis on 41 fruiting body forming Basidiomycete fungi and comparative transcriptome analysis during five developmental stages of four species of the Agaricales (Armillaria ostoyae, Coprinopsis cinerea, Schizophyllum commune, Auriculariopsis ampla) – two complex and two simplified fruiting body forming ones. Surprisingly the morphologically simplified organisms contain a higher number of TFs than most of the species with a more complex morphology. Examining the age distribution of TFs we discovered that genomes of simplified organisms contain the highest proportion of family or species specific regulator genes. Furthermore RNA-Seq data shows that these newly evolved genes play a crucial role during fruiting body formation – so their development is more dependent on evolutionarily young regulators. Our results contribute to a more comprehensive understanding of the development of mushroom fruiting bodies and to that of secondarily simplified species. The species we observed might be interesting examples of simplified morphology as an evolutionarily favorable attribute.