Evolution of Ty1 copy number control in yeast by horizontal transfer and recombination

Wioletta Czaja, Douda Bensasson, Hyo Won Ahn, David J. Garfinkel, Casey M. Bergman

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Abstract

Transposable elements constitute a large fraction of most eukaryotic genomes. Insertion of mobile DNA sequences typically has deleterious effects on host fitness, and thus diverse mechanisms have evolved to control mobile element proliferation. Mobility of the Ty1 retrotransposon in Saccharomyces yeasts is regulated by copy number control (CNC) mediated by a self-encoded restriction factor derived from the Ty1 gag capsid gene that inhibits viruslike particle function. Here, we survey a panel of wild and human-associated strains of S. cerevisiae and S. paradoxus to investigate how genomic Ty1 content influences variation in Ty1 mobility. We observe high levels of mobility for a tester element with a gag sequence from the canonical Ty1 subfamily in permissive strains that either lack full-length Ty1 elements or only contain full-length copies of the Ty1' subfamily that have a divergent gag sequence. In contrast, low levels of canonical Ty1 mobility are observed in restrictive strains carrying full-length Ty1 elements containing a canonical gag sequence. Phylogenomic analysis of full-length Ty1 elements revealed that Ty1' is the ancestral subfamily present in wild strains of S. cerevisiae, and that canonical Ty1 in S. cerevisiae is a derived subfamily that acquired gag from S. paradoxus by horizontal transfer and recombination. Our results provide evidence that variation in the ability of S. cerevisiae and S. paradoxus strains to repress canonical Ty1 transposition via CNC is regulated by the genomic content of different Ty1 subfamilies, and that self-encoded forms of transposon control can spread across species boundaries by horizontal transfer.

Original languageEnglish (US)
Article numbere1008632
JournalPLoS genetics
Volume16
Issue number2
DOIs
StatePublished - 2020

Bibliographical note

Funding Information:
This work was funded by the University of Georgia Research Foundation (DB, DJG and CMB), NERC NBAF award NBAF907 (DB), NIH grant R01GM095622 (DJG), and NIH grant R01GM124216 (DJG and CMB). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

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