Accessory genes are variably present among members of a species and are a reservoir of adaptive functions. In bacteria, differences in gene distributions among individuals largely result from mobile elements that acquire and disperse accessory genes as cargo. In contrast, the impact of cargo-carrying elements on eukaryotic evolution remains largely unknown. Here, we show that variation in genome content within multiple fungal species is facilitated by Starships, a newly discovered group of massive mobile elements that are 110 kb long on average, share conserved components, and carry diverse arrays of accessory genes. We identified hundreds of Starship-like regions across every major class of filamentous Ascomycetes, including 28 distinct Starships that range from 27-393 kb and last shared a common ancestor ca. 400 mya. Using new long-read assemblies of the plant pathogen Macrophomina phaseolina, we characterize 4 additional Starships whose activities contribute to standing variation in genome structure and content. One of these elements, Voyager, inserts into 5S rDNA and contains a candidate virulence factor whose increasing copy number has contrasting associations with pathogenic and saprophytic growth, suggesting Voyager’s activity underlies an ecological trade-off. We propose that Starships are eukaryotic analogs of bacterial integrative and conjugative elements based on parallels between their conserved components and may therefore represent the first dedicated agents of active gene transfer in eukaryotes. Our results suggest that Starships have shaped the content and structure of fungal genomes for millions of years and reveal a new concerted route for evolution throughout an entire eukaryotic phylum.

Accessory genes are variably present among members of a species and are a reservoir of adaptive functions. In bacteria, differences in gene distributions among individuals largely result from mobile elements that acquire and disperse accessory genes as cargo. In contrast, the impact of cargo-carrying elements on eukaryotic evolution remains largely unknown. Here, we show that variation in genome content within multiple fungal species is facilitated by Starships, a novel group of massive mobile elements that are 110 kb long on average, share conserved components, and carry diverse arrays of accessory genes. We identified hundreds of Starship-like regions across every major class of filamentous Ascomycetes, including 28 distinct Starships that range from 27-393 kb and last shared a common ancestor ca. 400 mya. Using new long-read assemblies of the plant pathogen Macrophomina phaseolina, we characterize 4 additional Starships whose past and ongoing activities contribute to standing variation in genome structure and content. One of these elements, Voyager, inserts into 5S rDNA and contains a candidate virulence factor whose increasing copy number has contrasting associations with pathogenic and saprophytic growth, suggesting Voyager activity underlies an ecological trade-off. We propose that Starships are eukaryotic analogs of bacterial integrative and conjugative elements based on parallels between their conserved components and may therefore represent the first known agents of active gene transfer in eukaryotes. Our results suggest that Starships have shaped the content and structure of fungal genomes for millions of years and reveal a new concerted route for evolution throughout an entire eukaryotic phylum.

Major quantitative disease resistance loci (QDRLs) are rare in the Phytophthora sojae (Kaufmann and Gerdemann)–soybean [Glycine max (L). Merr.] pathosystem. A major QDRL on chromosome 18 (QDRL‐18) was identified in PI 427105B and PI 427106. QDRL‐18 represents a valuable resistance source for breeding programs. Thus, our objectives were to determine its isolate specificity and measure its effect on yield and resistance to both P. sojae and other soybean pathogens. We characterized near isogenic lines (NILs) developed from F7 recombinant inbred lines heterozygous at QDRL‐18; NILs represent introgressions from PI 427105B, PI 427106, and susceptible ‘OX20‐8’. The introgressions from PI 427105B and PI 427106 increased resistance to P. sojae by 11 to 20% and 35 to 40%, respectively, based on laboratory and greenhouse assays, and increased yield by 13 to 29% under disease conditions. The resistant introgression from PI 427105B was also effective against seven P. sojae isolates with no isolate specificity detected. Based on quantitative polymerase chain reaction assays, NILs with the susceptible introgression had significantly higher relative levels of P. sojae colonization 48 h after inoculation. No pleiotropic effects for resistance to either soybean cyst nematode or Fusarium graminearum were detected. This information improves soybean breeders’ ability to make informed decisions regarding the deployment of QDRL‐18 in their respective breeding programs.

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