Transcriptional plasticity of schizotrophic Sclerotinia sclerotiorum responds to symptomatic rapeseed and endophytic wheat hosts

ABSTRACT Sclerotinia sclerotiorum, a widespread pathogen of dicotyledons, is also a reciprocal endophytic fungus in monocot plants. However, it is unclear how it responds to two distinct plants. Comparative transcriptomic analyses uncovered a network rewiring, with 14.1% up-differentially expressed genes overlapping upon colonizing the endophytic host wheat and a symptomatic host rapeseed. The divergent transcript of genes originating from host-specific induction is central to infection and colonization, including genes related to appressorium, oxalic acid, carbohydrate-active enzymes, and effector-like proteins. We confirmed that appressorium is required for S. sclerotiorum during colonization in symptomatic hosts but not in endophytic wheat via the observation of the infection process of ΔSs-caf1, a compound appressorium formation-defective mutant with hypovirulence to symptomatic hosts. SS1G_10617 and SS1G_13809 are components of the starch degradation pathways. ΔSS1G_10617 displayed lower virulence on symptomatic host plants and abnormal endophytic growth on wheat, and ΔSS1G_13809 only showed an abnormal symbiotic relationship with wheat, implying that starch may be the major carbon source for S. sclerotiorum in the symbiosis with wheat. Our results herein suggest that S. sclerotiorum modulates biphasic colonization via a divergent transcriptional landscape. This study contributes to a better understanding of schizotrophic fungi and provides new clues for cultivating disease-resistant varieties and adjusting reasonable farming strategies. IMPORTANCE The broad host range of fungi with differential fungal responses leads to either a pathogenic or an endophytic lifestyle in various host plants. Yet, the molecular basis of schizotrophic fungal responses to different plant hosts remains unexplored. Here, we observed a general increase in the gene expression of S. sclerotiorum associated with pathogenicity in symptomatic rapeseed, including small protein secretion, appressorial formation, and oxalic acid toxin production. Conversely, in wheat, many carbohydrate metabolism and transport-associated genes were induced, indicating a general increase in processes associated with carbohydrate acquisition. Appressorium is required for S. sclerotiorum during colonization in symptomatic hosts but not in endophytic wheat. These findings provide new clues for understanding schizotrophic fungi, fungal evolution, and the emergence pathways of new plant diseases. The broad host range of fungi with differential fungal responses leads to either a pathogenic or an endophytic lifestyle in various host plants. Yet, the molecular basis of schizotrophic fungal responses to different plant hosts remains unexplored. Here, we observed a general increase in the gene expression of S. sclerotiorum associated with pathogenicity in symptomatic rapeseed, including small protein secretion, appressorial formation, and oxalic acid toxin production. Conversely, in wheat, many carbohydrate metabolism and transport-associated genes were induced, indicating a general increase in processes associated with carbohydrate acquisition. Appressorium is required for S. sclerotiorum during colonization in symptomatic hosts but not in endophytic wheat. These findings provide new clues for understanding schizotrophic fungi, fungal evolution, and the emergence pathways of new plant diseases.