A FOX transcription factor phosphorylated for regulation of autophagy facilitates fruiting body development in Sclerotinia sclerotiorum

Summary Autophagy is a recycling process by which eukaryotic cells degrade their own components, and the fruiting body (sexual structure) is a necessary structure for some plant pathogenic fungi to start the infection cycle. However, the transcriptional regulation of plant pathogenic fungal autophagy and autophagy regulating sexual reproduction remains elusive. Here, we provide the report linking autophagy transcription and fruiting body development in phytopathogenic fungi. The forkhead box transcription factor (FOX TF) SsFoxE2 in Sclerotinia sclerotiorum (Ss) binds to the promoters of ATG genes, thus promoting their transcription. SsFoxE2 is phosphorylated by AMP‐activated protein kinase (AMPK) SsSnf1, and the phosphorylated SsFoxE2 interacts with (translationally controlled tumor protein) SsTctp1, leading to enhanced stability and ATG transcription activity of SsFoxE2. Importantly, the regulation of autophagy by SsFoxE2 affects the balance of the ubiquitination system and the early development of the fruiting body, which directly determines the occurrence and prevalence of plant disease. Furthermore, transcriptional binding of FOX TF to ATG gene promoters is conserved in phytopathogenic fungi. Taken together, our results bring new insights into pathogen initiation in phytopathogenic fungi and connect it to other autophagy‐regulated processes in plant pathogens.