Fungal hacking of the plant sex-determination pathway via interference with AGL24 in Silene latifolia

Plants have evolved lineage-specific sex-determination systems that is determined not only by genetic factors, but also the surrounding environmental conditions, including interactions with pathogens. Silene latifolia is a model dioecious plant whose sexuality is genetically regulated by X/Y chromosomes; however, anther smut fungus mimics the plant Y chromosome and forcibly converts female plants to male. Here, transcriptome analyses of healthy or fungus-infected S. latifolia inflorescence meristems suggested that an orthologue of AGL24 (SlAGL24), a flowering activator, is a key factor in sex conversion via fungus infection. Overexpression of SlAGL24 in Arabidopsis thaliana suppressed stamen development, whereas knock-down of SlAGL24 in S. latifolia converted males into hermaphrodites. Furthermore, SlAGL24 expression affected sexual dimorphisms in S. latifolia. Our results propose an adaptive scenario wherein the anther smut fungus targets SlAGL24, as a master regulator connecting the fungal signal to sex determination, to confer male and potentially male-beneficial traits, effectively transmitting its teliospores.