Transcriptome analysis of apple leaves infected by the rust fungus Gymnosporangium yamadae at two sporulation stages (spermogonia and aecia) reveals specific host responses, rust pathogenesis-related genes and a shift in the phyllosphere fungal community composition

Apple rustdisease caused by Gymnosporangium yamadaeis one of the major threats to apple orchards. In this study, dual RNA-seqanalysis was conducted to simultaneously monitor gene expression profiles of G. yamadae and infected apple leaves during the formation of rustspermogonia and aecia. The molecular mechanisms underlying this compatible interaction at 10 and 30 days post inoculation (dpi) indicate a significant reaction from the host plant and comprise detoxicationpathways at the earliest stage and the induction of secondary metabolismpathways at 30dpi. Such host reactions have been previously reported in other rust pathosystemsand may represent a general reaction to rustinfection. G. yamadae transcript profiling indicates a conserved geneticprogram in spermogonia and aecia that is shared with other rust fungi, whereas secretomeprediction reveals the presence of specific secreted candidate effector proteins expressed during apple infection. Unexpectedly, the survey of fungal unigenesin the transcriptome assemblies of inoculated and mock-inoculated apple leaves reveals that G. yamadae infection modifies the fungal community composition in the apple phyllosphereat 30 dpi. Collectively, our results provide novel insights into the compatible apple-apple rustinteraction and advance the knowledge of this heteroeciousdemicyclic rust fungus.