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

<jats:title>Abstract</jats:title><jats:p>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.<jats:italic>Silene latifolia</jats:italic>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<jats:italic>S. latifolia</jats:italic>inflorescence meristems suggested that an orthologue of<jats:italic>AGL24</jats:italic>(<jats:italic>SlAGL24</jats:italic>), a flowering activator, is a key factor in sex conversion<jats:italic>via</jats:italic>fungus infection. Overexpression of<jats:italic>SlAGL24</jats:italic>in<jats:italic>Arabidopsis thaliana</jats:italic>suppressed stamen development, whereas knock-down of<jats:italic>SlAGL24</jats:italic>in<jats:italic>S. latifolia</jats:italic>converted males into hermaphrodites. Furthermore,<jats:italic>SlAGL24</jats:italic>expression affected sexual dimorphisms in<jats:italic>S. latifolia</jats:italic>. Our results propose an adaptive scenario wherein the anther smut fungus targets<jats:italic>SlAGL24</jats:italic>, as a master regulator connecting the fungal signal to sex determination, to confer male and potentially male-beneficial traits, effectively transmitting its teliospores.</jats:p>