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The insertion of a mitochondrial selfish element into the nuclear genome and its consequences

View ORCID ProfileJulien Y. Dutheil, Karin Münch, View ORCID ProfileKlaas Schotanus, View ORCID ProfileEva H. Stukenbrock, View ORCID ProfileRegine Kahmann
doi: https://doi.org/10.1101/787044
Julien Y. Dutheil
1Max Planck Institute for Evolutionary Biology – Plön, Germany
2Max Planck Institute for Terrestrial Microbiology – Marburg, Germany
3Institute of Evolutionary Sciences CNRS – University of Montpellier – IRD – EPHE – Montpellier, France
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  • For correspondence: dutheil@evolbio.mpg.de
Karin Münch
2Max Planck Institute for Terrestrial Microbiology – Marburg, Germany
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Klaas Schotanus
2Max Planck Institute for Terrestrial Microbiology – Marburg, Germany
4Christian Albrechts University of Kiel – Kiel, Germany
5Department of Molecular Genetics and Microbiology (MGM). Duke University Medical Center – Durham, NC, USA
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Eva H. Stukenbrock
1Max Planck Institute for Evolutionary Biology – Plön, Germany
2Max Planck Institute for Terrestrial Microbiology – Marburg, Germany
4Christian Albrechts University of Kiel – Kiel, Germany
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Regine Kahmann
2Max Planck Institute for Terrestrial Microbiology – Marburg, Germany
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Abstract

Homing endonucleases (HE) are enzymes capable of cutting DNA at highly specific target sequences, the repair of the generated double-strand break resulting in the insertion of the HE-encoding gene (“homing” mechanism). HEs are present in all three domains 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 accidentally integrated into a telomeric region of the nuclear genome 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 from a different species. The telomeric HE underwent mutations in its active site and lost its original start codon. A potential other start codon was retained downstream, but we did not detect any significant transcription of the newly created open reading frame, suggesting that the inserted gene is not functional. Besides, 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 mutational event altered two genes: the integrated HE gene subsequently lost its homing activity, while its insertion created a truncated version of an existing gene, possibly altering its function. As the insertion is absent in other field isolates, suggesting that it is recent, the U. maydis 521 reference strain offers a snapshot of this singular mutational event.

Competing Interest Statement

The authors have declared no competing interest.

Footnotes

  • Footnote: Version 4 of this preprint has been peer-reviewed and recommended by Peer Community In Evolutionary Biology (https://doi.org/10.24072/pci.evolbiol.100101)

  • This update contains formatting adjustments and correction of typos.

  • https://gitlab.gwdg.de/molsysevol/umag_11064

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-NC-ND 4.0 International license.
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Posted May 16, 2020.
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The insertion of a mitochondrial selfish element into the nuclear genome and its consequences
Julien Y. Dutheil, Karin Münch, Klaas Schotanus, Eva H. Stukenbrock, Regine Kahmann
bioRxiv 787044; doi: https://doi.org/10.1101/787044
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The insertion of a mitochondrial selfish element into the nuclear genome and its consequences
Julien Y. Dutheil, Karin Münch, Klaas Schotanus, Eva H. Stukenbrock, Regine Kahmann
bioRxiv 787044; doi: https://doi.org/10.1101/787044

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