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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.