Fungal hacking of the plant sex-determination pathway via interference withAGL24inSilene latifolia

Abstract 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.