Giant Starship Elements Mobilize Accessory Genes in Fungal Genomes

Gluck-Thaler, Emile; Ralston, Timothy; Konkel, Zachary; Ocampos, Cristhian Grabowski; Ganeshan, Veena Devi; Dorrance, Anne E.; Niblack, Terry L.; Wood, Corlett W.; Slot, Jason C.; Lopez-Nicora, Horacio D.; Vogan, Aaron A.

doi:10.1093/molbev/msac109

Title: Giant Starship Elements Mobilize Accessory Genes in Fungal Genomes

Journal Article · 19 May 2022 · Molecular Biology and Evolution

DOI: https://doi.org/10.1093/molbev/msac109 · OSTI ID:1904111

^[1]; Ralston, Timothy ^[2]; Konkel, Zachary ^[2]; Ocampos, Cristhian Grabowski ^[3]; Ganeshan, Veena Devi ^[2]; Dorrance, Anne E. ^[2]; Niblack, Terry L. ^[2]; Wood, Corlett W. ^[4];

^[2]; Lopez-Nicora, Horacio D. ^[2];

^[5]

University of Pennsylvania, Philadelphia, PA (United States); The Ohio State University, Columbus, OH (United States); OSTI
The Ohio State University, Columbus, OH (United States)
Universidad Nacional de Asunción, San Lorenzo (Paraguay)
University of Pennsylvania, Philadelphia, PA (United States)
Uppsala University (Sweden)

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 to 393 kb and last shared a common ancestor ca. 400 Ma. Using new long-read assemblies of the plant pathogen Macrophomina phaseolina, we characterize four 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.

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Research Organization:: USDOE Joint Genome Institute (JGI), Berkeley, CA (United States)

Sponsoring Organization:: Marie Skłodowska-Curie Foundation; National Science Foundation (NSF); Ohio Soybean Council; Swedish Research Council; USDOE Office of Science (SC)

Grant/Contract Number:: AC02-05CH11231

OSTI ID:: 1904111

Journal Information:: Molecular Biology and Evolution, Journal Name: Molecular Biology and Evolution Journal Issue: 5 Vol. 39; ISSN 0737-4038

Publisher:: Oxford University PressCopyright Statement

Country of Publication:: United States

Language:: English

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The RIPper, a web-based tool for genome-wide quantification of Repeat-Induced Point (RIP) mutations van Wyk, Stephanie; Harrison, Christopher H.; Wingfield, Brenda D. PeerJ, Vol. 7 https://doi.org/10.7717/peerj.7447	journal	January 2019

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59 BASIC BIOLOGICAL SCIENCES
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