Basidiomycete fruiting body morphology correlates with the convergent loss of photolyase-related proteins

Abstract

Summary Cryptochromes and photolyase-related (CRY/PHR) proteins are flavoproteins involved in blue-light signaling and/or the light-dependent repair of UV-induced DNA damage across all domains of life. Although well-studied in many eukaryotes, their evolution and function in mushroom-forming fungi (Agaricomycetes and Basidiomycota) remain poorly understood. By analyzing 655 genomes, we show that fungi ancestrally possessed four CRY/PHR subfamilies, of which class I cyclobutane pyrimidine dimer (CPD) photolyases became broadly conserved across Dikarya. Class I CPD photolyase-related proteins have been lost in Agaricomycetes with gasteroid fruiting bodies, where sexual spores develop shielded from light. Functional characterization of the class I CPD protein Phr1 of Coprinopsis cinerea confirmed its light-dependent photorepair function. We further demonstrated that phr1 expression is upregulated by blue light in a white-collar-complex-dependent manner. Overall, our results provide an example of parallel gene loss associated with a morphological change and shed new light on the evolution of the CRY/PHR protein family.