1. Evolutionary Biology
  2. Genetics and Genomics

The effect of hybridization on transposable element accumulation in an undomesticated fungal species

  1. Mathieu Hénault  Is a corresponding author
  2. Souhir Marsit
  3. Guillaume Charron
  4. Christian R Landry
  1. Université Laval, Canada
https://doi.org/10.7554/eLife.60474
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  1. Mathieu Hénault
  2. Souhir Marsit
  3. Guillaume Charron
  4. Christian R Landry
(2020)
The effect of hybridization on transposable element accumulation in an undomesticated fungal species
eLife 9:e60474.
https://doi.org/10.7554/eLife.60474
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Abstract

Transposable elements (TEs) are mobile genetic elements that can profoundly impact the evolution of genomes and species. A long-standing hypothesis suggests that hybridization could deregulate TEs and trigger their accumulation, although it received mixed support from studies in plants and animals. Here, we tested this hypothesis in fungi using incipient species of the undomesticated yeast Saccharomyces paradoxus. Population genomic data revealed no signature of higher transposition in natural hybrids. As we could not rule out the elimination of past transposition increase signatures by natural selection, we performed a laboratory evolution experiment on a panel of artificial hybrids to measure TE accumulation in the near absence of selection. Changes in TE copy numbers were not predicted by the level of evolutionary divergence between the parents of a hybrid genotype. Rather, they were highly dependent on the individual hybrid genotypes, showing that strong genotype-specific deterministic factors govern TE accumulation in yeast hybrids.

Data availability

Illumina short read sequencing data of the MA lines is available at NCBI under accession PRJNA515073. Genome assemblies and Nanopore long read sequencing data of wild isloates are available at NCBI under accession PRJNA514804. Illumina short read sequencing data of wild isolates is available at NCBI under accessions PRJNA277692, PRJNA324830 and PRJNA479851.

The following data sets were generated
The following previously published data sets were used

Article and author information

Author details

  1. Mathieu Hénault

    Département de biochimie, microbiologie et bio-informatique, Département de biologie, PROTEO, BDRC_UL, Université Laval, Québec, Canada
    For correspondence
    mathieu.henault.1@ulaval.ca
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-0760-7545

  2. Souhir Marsit

    Département de biochimie, microbiologie et bio-informatique, PROTEO, BDRC_UL, Université Laval, Québec, Canada
    Competing interests
    No competing interests declared.

  3. Guillaume Charron

    Département de biologie, PROTEO, BDRC_UL, Université Laval, Québec, Canada
    Competing interests
    No competing interests declared.

  4. Christian R Landry

    Département de biologie, Université Laval, Québec, Canada
    Competing interests
    Christian R Landry, Reviewing editor, eLife.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-3028-6866

Funding

Natural Sciences and Engineering Research Council of Canada (RGPIN-2015-03755)

  • Christian R Landry

Natural Sciences and Engineering Research Council of Canada (NSERC Alexander Graham-Bell doctoral scholarship)

  • Mathieu Hénault
  • Guillaume Charron

Fonds de recherche du Québec – Nature et technologies (FRQNT doctoral scholarship)

  • Mathieu Hénault
  • Guillaume Charron

Fonds de Recherche du Québec - Santé (FRQS postdoctoral scholarship)

  • Souhir Marsit

Canada Research Chairs (Canada Research Chair in Evolutionary Cell and Systems Biology)

  • Christian R Landry

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

Copyright

© 2020, Hénault 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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  1. Mathieu Hénault
  2. Souhir Marsit
  3. Guillaume Charron
  4. Christian R Landry
(2020)
The effect of hybridization on transposable element accumulation in an undomesticated fungal species
eLife 9:e60474.
https://doi.org/10.7554/eLife.60474

Share this article

https://doi.org/10.7554/eLife.60474

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Further reading

    1. Genetics and Genomics

    The genomic landscape of transposable elements in yeast hybrids is shaped by structural variation and genotype-specific modulation of transposition rate

    Mathieu Hénault, Souhir Marsit ... Christian R Landry
    Research Advance

    Transposable elements (TEs) are major contributors to structural genomic variation by creating interspersed duplications of themselves. In return, structural variants (SVs) can affect the genomic distribution of TE copies and shape their load. One long-standing hypothesis states that hybridization could trigger TE mobilization and thus increase TE load in hybrids. We previously tested this hypothesis (Hénault et al., 2020) by performing a large-scale evolution experiment by mutation accumulation (MA) on multiple hybrid genotypes within and between wild populations of the yeasts Saccharomyces paradoxus and Saccharomyces cerevisiae. Using aggregate measures of TE load with short-read sequencing, we found no evidence for TE load increase in hybrid MA lines. Here, we resolve the genomes of the hybrid MA lines with long-read phasing and assembly to precisely characterize the role of SVs in shaping the TE landscape. Highly contiguous phased assemblies of 127 MA lines revealed that SV types like polyploidy, aneuploidy, and loss of heterozygosity have large impacts on the TE load. We characterized 18 de novo TE insertions, indicating that transposition only has a minor role in shaping the TE landscape in MA lines. Because the scarcity of TE mobilization in MA lines provided insufficient resolution to confidently dissect transposition rate variation in hybrids, we adapted an in vivo assay to measure transposition rates in various S. paradoxus hybrid backgrounds. We found that transposition rates are not increased by hybridization, but are modulated by many genotype-specific factors including initial TE load, TE sequence variants, and mitochondrial DNA inheritance. Our results show the multiple scales at which TE load is shaped in hybrid genomes, being highly impacted by SV dynamics and finely modulated by genotype-specific variation in transposition rates.