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

Abstract

AbstractPlants 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 latifoliais 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-infectedS. latifoliainflorescence meristems suggested that an orthologue ofAGL24(SlAGL24), a flowering activator, is a key factor in sex conversionviafungus infection. Overexpression ofSlAGL24inArabidopsis thalianasuppressed stamen development, whereas knock-down ofSlAGL24inS. latifoliaconverted males into hermaphrodites. Furthermore,SlAGL24expression affected sexual dimorphisms inS. latifolia. Our results propose an adaptive scenario wherein the anther smut fungus targetsSlAGL24, as a master regulator connecting the fungal signal to sex determination, to confer male and potentially male-beneficial traits, effectively transmitting its teliospores.