Dynamics of Ophiostoma novo-ulmi transcriptome during colonization of resistant and susceptible Ulmus minor hosts

Dutch elm disease (DED), caused by Ophiostoma novo-ulmi , is still one of the most devastating forest diseases worldwide. Natural variation among Ulmus minor genotypes provides an opportunity to investigate how the pathogen modulates its infection strategy in resistant versus susceptible hosts. Using RNA-Seq, we comprehensively profiled the transcription of a virulent O. novo-ulmi strain during colonization of three U. minor genotypes, two resistant (R-VAD2 and R-MDV2.3) and one susceptible (S-MDV1), sampling local and distal stem tissues at four time points post-inoculation. Differential expression analysis relative to the earliest sampling time identified 178 fungal differentially expressed genes (DEGs), of which 15% showed homology to PHI (Pathogen–Host Interactions) database entries associated with virulence and effector-function phenotypes in other pathosystems. This DEG set displayed a shared transcriptional pattern across host genotypes, dominated by secondary metabolism, redox activity, and host compound modification. Beyond this shared response, fungal gene expression diverged depending on the host genotype, with the strongest differences observed at 72 hours post-inoculation. In R-VAD2, O. novo-ulmi exhibited pronounced host-induced adjustments characterized by stress-related and cell-wall-interacting functions. In R-MDV2.3, O. novo-ulmi adopted an attenuated expression program dominated by detoxification and solute transport. In contrast, colonization of the susceptible genotype S-MDV1 triggered a slower but broader oxidoreductase-centered response that peaked later. Notably, fungal transcript detection was higher in the susceptible genotype, likely facilitated by anatomical traits previously associated with increased vulnerability to vascular pathogens. This work provides new mechanistic insights into how O. novo-ulmi colonizes and interacts with its host, exposing striking differences not only between susceptible and resistant hosts but also within resistant genotypes.