An evolutionarily ancient transcription factor drives spore morphogenesis in mushroom-forming fungi

Sporulation is the most widespread means of reproduction and dispersal in fungi and, at the same time, an industrially important trait in crop mushrooms. In the Basidiomycota, sexual spores are produced on specialized cells known as basidia, from which they are forcibly discharged with the highest known acceleration in nature. However, the genetics of sporulation remains poorly known. Here, we identify a new, highly conserved transcription factor, sporulation-related regulator 1 (srr1), and systematically address the genetics of spore formation for the first time in the Basidiomycota. We show that Srr1 regulates postmeiotic spore morphogenesis, but not other aspects of fruiting body development or meiosis, and its role is conserved in the phylogenetically distant, but industrially important, Pleurotus spp. (oyster mushrooms). We used RNA sequencing to understand genes directly or indirectly regulated by Srr1 and identified a strongly supported binding motif for the protein. Using an inferred network of putative target genes regulated by Srr1 and comparative genomics, we identified genes lost in secondarily non-ballistosporic taxa, including a novel sporulation-specific chitinase gene. Overall, our study offers systematic insights into the genetics of spore morphogenesis in the Basidiomycota.