Rum1 and Cdc73 integrate transcriptional repression and autophagy to control teliospore timing in Ustilago maydis.

Abstract

In the biotrophic smut fungus Ustilago maydis, teliospore formation depends on mating and host cues, but the mechanisms that restrain this program during vegetative growth remain unclear. We show that loss of the conserved PAF1 complex subunit UmCdc73 triggers spontaneous teliospore-like differentiation under axenic conditions. The resulting structures undergo cellular remodeling, wall thickening and melanization, acquire increased heat tolerance and limited germination capacity, and induce meiosis-related genes during germination. UmRum1 directly binds to the UmCDC73 promoter and represses its activity, whereas UmCdc73 physically associates with the core autophagy factor UmAtg5. Genetic analysis places UmCDC73 downstream of UmRUM1 in controlling the axenic phenotype. Loss of UmCDC73 also prematurely activates teliospore- and late-infection-associated transcriptional programs and is accompanied by increased maize defense marker expression and reduced virulence. At 120 h, the Δumcdc73Δatg5 double mutant showed less advanced differentiation than Δumcdc73, supporting a contribution of UmAtg5-dependent autophagy to efficient differentiation-associated cellular remodeling. Together, these findings identify UmCdc73 as a developmental checkpoint and connect Rum1-dependent transcriptional repression with autophagy-associated remodeling to coordinate developmental timing and pathogenic fitness.