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The yeast mating-type switching endonuclease HO is a domesticated member of an unorthodox homing genetic element family

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Cite this article as: eLife 2020;9:e55336 doi: 10.7554/eLife.55336

Abstract

The mating-type switching endonuclease HO plays a central role in the natural life cycle of Saccharomyces cerevisiae, but its evolutionary origin is unknown. HO is a recent addition to yeast genomes, present in only a few genera close to Saccharomyces. Here we show that HO is structurally and phylogenetically related to a family of unorthodox homing genetic elements found in Torulaspora and Lachancea yeasts. These WHO elements home into the aldolase gene FBA1, replacing its 3' end each time they integrate. They resemble inteins but they operate by a different mechanism that does not require protein splicing. We show that a WHO protein cleaves Torulaspora delbrueckii FBA1 efficiently and in an allele-specific manner, leading to DNA repair by gene conversion or NHEJ. The DNA rearrangement steps during WHO element homing are very similar to those during mating-type switching, and indicate that HO is a domesticated WHO-like element.

Article and author information

Author details

  1. Aisling Y Coughlan

    UCD Conway Institute, University College Dublin, Dublin, Ireland
    Competing interests
    The authors declare that no competing interests exist.
  2. Lisa Lombardi

    UCD Conway Institute, University College Dublin, Dublin, Ireland
    Competing interests
    The authors declare that no competing interests exist.
  3. Stephanie Braun-Galleani

    UCD Conway Institute, University College Dublin, Dublin, Ireland
    Competing interests
    The authors declare that no competing interests exist.
  4. Alexandre AR Martos

    UCD Conway Institute, University College Dublin, Dublin, Ireland
    Competing interests
    The authors declare that no competing interests exist.
  5. Virginie Galeote

    SPO, INRAE, Montpellier, France
    Competing interests
    The authors declare that no competing interests exist.
  6. Frédéric Bigey

    SPO, INRAE, Montpellier, France
    Competing interests
    The authors declare that no competing interests exist.
  7. Sylvie Dequin

    SPO, INRAE, Montpellier, France
    Competing interests
    The authors declare that no competing interests exist.
  8. Kevin P Byrne

    UCD Conway Institute, University College Dublin, Dublin, Ireland
    Competing interests
    The authors declare that no competing interests exist.
  9. Kenneth H Wolfe

    UCD Conway Institute, University College Dublin, Dublin, Ireland
    For correspondence
    kenneth.wolfe@ucd.ie
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-4992-4979

Funding

Science Foundation Ireland (13/IA/1910)

  • Kenneth H Wolfe

European Research Council (789341)

  • Kenneth H Wolfe

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Reviewing Editor

  1. Alan M Moses, University of Toronto, Canada

Publication history

  1. Received: January 21, 2020
  2. Accepted: April 24, 2020
  3. Accepted Manuscript published: April 27, 2020 (version 1)

Copyright

© 2020, Coughlan et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

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