Annotated genome assemblies for Arachnopeziza aurata and Arachnopeziza aurelia

Obligate biotrophic pathogens like the phytopathogenic powdery mildew fungi commit to a closely dependent relationship with their plant hosts and have lost the ability to survive and reproduce independently. Thus, at present these organisms are not amenable to in vitro cultivation, which is required for effective genetic modification and functional molecular studies. Saprohytic fungi of the family Arachnopezizaceae are the closest known extant relatives of the powdery mildew fungi. We hypothesize that these fungi hold great potential for studying genetic components of their obligate biotrophic lifestyle. In this work, we established telomere-to-telomere genome assemblies for two representatives of this family, Arachnopeziza aurata and A. aurelia. We discovered that in contrast to the powdery mildews, these fungi possess compact genomes with a repeat content below 5% and signs of functioning repeat-induced point mutation (RIP) to limit TE spread. We succeeded in cultivating both fungal species in liquid and on solid standard media and show that they are sensitive to common fungicides such as hygromycin and fenhexamid. Further, we were able to use a standard protocol for the genetic modification of fungi, polyethelene glycol-mediated protoplast transformation, to confer hygromycin resistance and express a red fluorescent protein in the species A. aurata. Overall, we demonstrated that Arachnopeziza species are amenable to genetic alterations that may include gene replacement, gene modification, and gene complementation in the future. We established a potential model system that promises to sidestep the need for genetic modification of powdery mildew fungi by using Arachnopeziza species as a proxy. Our work also provides high-quality genomic resources for A. aurata and A. aurelia, which will be valuable for the fungal research community.