Evolutionary genomics reveals variation in structure and genetic content implicated in virulence and lifestyle in the genus Gaeumannomyces

Abstract Gaeumannomyces tritici is responsible for take-all disease, one of the most important wheat root threats worldwide. High-quality annotated genome resources are sorely lacking for this pathogen, as well as for the closely related antagonist and potential wheat take-all biocontrol agent, G. hyphopodioides. As such, we know very little about the genetic basis of the interactions in this host–pathogen–antagonist system. Using PacBio HiFi sequencing technology we have generated nine near-complete assemblies, including two different virulence lineages for G. tritici and the first assemblies for G. hyphopodioides and G. avenae (oat take-all). Genomic signatures support the presence of two distinct virulence lineages in G. tritici (types A and B), with A strains potentially employing a mechanism to prevent gene copy-number expansions. The CAZyme repertoire was highly conserved across Gaeumannomyces, while candidate secreted effector proteins and biosynthetic gene clusters showed more variability and may distinguish pathogenic and non-pathogenic lineages. A transition from self-sterility (heterothallism) to self-fertility (homothallism) may also be a key innovation implicated in lifestyle. We did not find evidence for transposable element and effector gene compartmentalisation in the genus, however the presence of Starship giant transposable elements may contribute to genomic plasticity in the genus. Our results depict Gaeumannomyces as an ideal system to explore interactions within the rhizosphere, the nuances of intraspecific virulence, interspecific antagonism, and fungal lifestyle evolution. The foundational genomic resources provided here will enable the development of diagnostics and surveillance of understudied but agriculturally important fungal pathogens.