The yeast mating-type switching endonuclease HO is a domesticated member of an unorthodox homing genetic element family
- University College Dublin, Ireland
- INRAE, France
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.
Data availability
Key nucleotide sequence data is provided in Supplementary File 1. New genome sequences have been deposited at NCBI. Their Bioproject numbers are in the dataset table and also in Supplementary files 1 and 2 of the manuscript.
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Torulaspora franciscae genome sequencingNCBI Bioproject, PRJNA622240.
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Torulaspora delbrueckii genome sequencingNCBI Bioproject, PRJNA623898.
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Torulaspora delbrueckii strain:NCYC696 Genome sequencingNCBI Bioproject, PRJNA623891.
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Torulaspora pretoriensis genome sequencingNCBI Bioproject, PRJNA623867.
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Torulaspora globosa CBS764 genome sequencing and assemblyNCBI Bioproject, PRJNA625704.
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Torulaspora globosa CBS2947 genome sequencing and assemblyNCBI Bioproject, PRJNA625705.
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Naumovozyma castellii genome sequencingNCBI Bioproject, PRJNA623732.
Article and author information
Author details
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
- Alan M Moses, University of Toronto, Canada
Version history
- Received: January 21, 2020
- Accepted: April 24, 2020
- Accepted Manuscript published: April 27, 2020 (version 1)
- Version of Record published: June 9, 2020 (version 2)
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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The yeast mating-type switching endonuclease HO is a domesticated member of an unorthodox homing genetic element family
eLife 9:e55336.
https://doi.org/10.7554/eLife.55336
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