Effector gene reshuffling involves dispensable mini-chromosomes in the wheat blast fungus

Author summary The emerging blast disease on wheat is proving even harder to control than the ancient, still-problematic rice blast disease. Potential wheat resistance identified using strains isolated soon after disease emergence are no longer effective in controlling recent aggressive field isolates from wheat in South America and South Asia. We construct a high-quality assembly of an aggressive, recently-isolated wheat blast fungal strain and the first assembled mini-chromosome genome sequence of wheat and rice blast pathogens. We report that recent wheat pathogens can contain one or two highly-variable dispensable mini-chromosomes, each with an amalgamation of fungal effector genes and other sequences that are duplicated or absent from indispensable core chromosome ends. Well-studied effectors found on different core chromosomes in rice pathogens appear side-by-side in wheat pathogen mini-chromosomes. The rice pathogen often overcomes deployed resistance genes by deleting triggering effector genes. We propose that the fast-evolving effector-rich compartment of the wheat blast fungus is a combination of core chromosome ends and mobile mini-chromosomes that are easily lost from individual strains. Localization of effectors on mini-chromosomes would therefore accelerate pathogen adaptation in the field. Newly emerged wheat blast disease is a serious threat to global wheat production. Wheat blast is caused by a distinct, exceptionally diverse lineage of the fungus causing rice blast disease. Through sequencing a recent field isolate, we report a reference genome that includes seven core chromosomes and mini-chromosome sequences that harbor effector genes normally found on ends of core chromosomes in other strains. No mini-chromosomes were observed in an early field strain, and at least two from another isolate each contain different effector genes and core chromosome end sequences. The mini-chromosome is enriched in transposons occurring most frequently at core chromosome ends. Additionally, transposons in mini-chromosomes lack the characteristic signature for inactivation by repeat-induced point (RIP) mutation genome defenses. Our results, collectively, indicate that dispensable mini-chromosomes and core chromosomes undergo divergent evolutionary trajectories, and mini-chromosomes and core chromosome ends are coupled as a mobile, fast-evolving effector compartment in the wheat pathogen genome.