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The transfer of a mitochondrial selfish element to the nuclear genome and its consequences

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Dutheil,  Julien Y.
Research Group Molecular Systems Evolution, Department Evolutionary Genetics, Max Planck Institute for Evolutionary Biology, Max Planck Society;

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Stukenbrock,  Eva H.
Max Planck Fellow Group Environmental Genomics, Max Planck Institute for Evolutionary Biology, Max Planck Society;

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Dutheil, J. Y., Münch, K., Schotanus, K., Stukenbrock, E. H., & Kahmann, R. (2019). The transfer of a mitochondrial selfish element to the nuclear genome and its consequences. bioRxiv. doi:10.1101/787044.


Cite as: http://hdl.handle.net/21.11116/0000-0005-1058-6
Abstract
Homing endonucleases (HE) are enzymes capable of excising their encoding gene and inserting it in a highly specific target sequence. As such, they act both as intronic sequences (type-I introns) and selfish invasive elements. HEs are present in all three kingdoms of life and viruses; in eukaryotes, they are mostly found in the genomes of mitochondria and chloroplasts, as well as nuclear ribosomal RNAs. We here report the case of a HE that integrated into a telomeric region of the fungal maize pathogen Ustilago maydis. We show that the gene has a mitochondrial origin, but its original copy is absent from the U. maydis mitochondrial genome, suggesting a subsequent loss or a horizontal transfer. The telomeric HE underwent mutations in its active site and acquired a new start codon, but we did not detect significant transcription of the newly created open reading frame. The insertion site is located in a putative RecQ helicase gene, truncating the C-terminal domain of the protein. The truncated helicase is expressed during infection of the host, together with other homologous telomeric helicases. This unusual homing event represents a singular evolutionary time point: the creation of two new genes whose fate is not yet written. The HE gene lost its homing activity and can potentially acquire a new function, while its insertion created a truncated version of an existing gene, possibly altering its original function.