Abstract
The ascomycete fungus Ophiostoma novo-ulmi is responsible for the pandemic of Dutch elm disease that has been ravaging Europe and North America for 50 years. We proceeded to annotate the genome of the O. novo-ulmi strain H327 that was sequenced in 2012. The 31.784-Mb nuclear genome (50.1% GC) is organized into 8 chromosomes containing a total of 8,640 protein-coding genes that we validated with RNA sequencing analysis. Approximately 53% of these genes have their closest match to Grosmannia clavigera kw1407, followed by 36% in other close Sordariomycetes, 5% in other Pezizomycotina, and surprisingly few (5%) orphans. A relatively small portion (~3.4%) of the genome is occupied by repeat sequences; however, the mechanism of repeat-induced point mutation appears active in this genome. Approximately 76% of the proteins could be assigned functions using Gene Ontology analysis; we identified 311 carbohydrate-active enzymes, 48 cytochrome P450s, and 1,731 proteins potentially involved in pathogen– host interaction, along with 7 clusters of fungal secondary metabolites. Complementary mating-type locus sequencing, mating tests, and culturing in the presence of elm terpenes were conducted. Our analysis identified a specific genetic arsenal impacting the sexual and vegetative growth, phytopathogenicity, and signaling/plant–defense–degradation relationship between O. novo-ulmi and its elm host and insect vectors. Introduction During the last centuries, increased movements of people and goods across countries and continents have favored the emergence and global spread of plant pathogens, insect pests, and invasive weeds which have substantially altered the landscape of several parts of the world. One well-documented example is Dutch elm disease (DED), the most destructive disease of elms. It has been estimated that over 1 billion mature elms were killed by two successive pandemics since the early 1900s (Paoletti et al. 2005). The first pandemic, which prompted initial investigations by Dutch scientists shortly after the First World War (Holmes and Heybroek 1990), was caused by the ascomycete fungus Ophiostoma ulmi (Buisman) Nannf. As it spread relentlessly over Western Europe and, a few decades