Coordinated Gene Family Evolution Shapes the Genome of Dimorphic Organisms

Abstract Dimorphic organisms possess the remarkable genome capacity to alternate genetic information between two distinct life forms 1,2 . In dimorphic fungi, yeast and mycelium can reversibly transition as a function of environmental stimuli 3,4 . However, the evolutionary solution that allows for the integration of genetic information from two divergent life forms into a single dimorphic organism remains unresolved. Here, we report hundreds of gene families exhibiting convergent evolution to adapt their paralogs to dimorphism. This adaptation involves paralog functionalization and the coordination of their expression, with yeast and mycelium-specific paralogs. Though these families have distinct functions, all their paralogs are convergently adapted to yeast and mycelium morphologies. In addition, dimorphic gene families with related functions form head-to-head structures, further coordinating differential expression. This coordinated regulation is controlled by two new genes, dkl and dfl . Loss of function of these genes results in global dysregulation of gene expression and loss of dimorphism. Dimorphic gene families, head-to-head marker loci, and the dfl gene are conserved across various dimorphic species but are absent in closely related monomorphic species. Our findings represent a novel evolutionary mechanism that integrates and optimizes the genetic information required for two distinct life forms within a single organism.