Coordinated gene family evolution shapes the genome of dimorphic Mucorales

Dimorphic organisms possess the remarkable genome capacity to alternate genetic information between two distinct life forms. In dimorphic Mucorales, lineages can reversibly transition between yeast and mycelium as a function of environmental stimuli. However, how genetic information produces two divergent life evolves in a single genome remains unresolved. Here, we report hundreds of gene families exhibiting convergent evolution for dimorphism. This adaptation involves paralog functionalization and the coordination of expression, with yeast and mycelium-specific paralogs. Though these gene families have distinct functions, all their paralogs are convergently adapted to produce yeast and mycelium morphologies. In addition, dimorphic gene families with related functions form head-to-head structures, 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 identify an evolutionary mechanism that integrates and optimizes the genetic information required for two distinct life forms within a single organism. Dimorphic organisms switch between two distinct life forms, but how a single genome controls the genetic program for both states is unclear. The study identifies hundreds of convergently evolved gene families and two regulator genes, dkl and dfl, that coordinate expression to optimize the two morphologies of Mucorales fungi.