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

Hénault, Mathieu; Marsit, Souhir; Charron, Guillaume; Landry, Christian R.

doi:10.7554/elife.60474

Cited by 31 publications

(53 citation statements)

References 128 publications

(159 reference statements)

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“…Estimates of mutation rates for the same cross types are largely consistent, and inter-lineage crosses (BC, 2% parental divergence) have mutation rates similar to intra-lineage crosses (BB and CC), suggesting that the level of divergence between parental genomes does not influence mutation rate. This is consistent with the results of (Hénault et al 2020) who found no relationship between the activity of transposable elements and the level of divergence between parental genomes in the same crosses. Overall, our results suggest that lineage-specific mutation rates and genotype-specific factors contribute most to differences in mutation rates and spectra among hybrid crosses of different levels of parental divergence.…”

Section: Resultssupporting

confidence: 93%

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Heterogeneous mutation rates and spectra in yeast hybrids

Fijarczyk

Hénault

Marsit

et al. 2021

Preprint

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Mutation rates and spectra vary between species and among populations. Hybridization can contribute to this variation but its role remains poorly understood. Estimating mutation rates requires controlled conditions where the effect of natural selection can be minimized. One way to achieve this is through mutation accumulation experiments coupled with genome sequencing. Here we investigate 400 mutation accumulation lines initiated from 11 genotypes spanning intra-lineage, inter-lineage and interspecific crosses of the yeasts Saccharomyces paradoxus and S. cerevisiae, and propagated for 770 generations. We find significant differences in mutation rates and spectra among crosses, which are not related to the level of divergence of parental strains, but are genotype specific. We find that departures from neutrality, differences in growth rate, ploidy and loss of heterozygosity only play a minor role as a source of variation and conclude that unique combinations of parental genotypes drive distinct rates and spectra in some crosses.

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Section: Resultssupporting

confidence: 93%

“…. paradoxus SpA, SpB and SpC parents, the gene predictions, and annotations of representative strains (LL2012_001, MSH-604 and LL2011_012 respectively) from(Hénault et al 2020) were used. For S. cerevisiae, genome annotations of the strain YPS128 from(Yue et al 2017) were used.…”

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confidence: 99%

Heterogeneous mutation rates and spectra in yeast hybrids

Fijarczyk

Hénault

Marsit

et al. 2021

Preprint

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“…Furthermore, there is growing evidence that hybridization events and their associated TE contents is not obligatory subjected to massive TE deregulation. Such outcomes were described in yeast species [57,58], as well as in other groups including plants [59,60] and insects [61,62].…”

Section: Resultsmentioning

confidence: 83%

Species-wide transposable element repertoires retrace the evolutionary history of the Saccharomyces cerevisiae host

Bleykasten-Grosshans

Fabrizio

Friedrich

et al. 2021

Preprint

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Transposable elements (TE) are an important source of genetic variation with a dynamic and content that greatly differ in a wide range of species. The origin of the intraspecific content variation is not always clear and little is known about the precise nature of it. Here, we surveyed the species-wide content of the Ty LTR-retrotransposons in a broad collection of 1,011 Saccharomyces cerevisiae natural isolates to understand what can stand behind the variation of the repertoire, i.e. the type and number of Ty elements. We have compiled an exhaustive catalog of all TE variants present in the S. cerevisiae species by identifying a large set of new variants. The characterization of the TE content in each isolate clearly highlighted that each subpopulation exhibits a unique and specific repertoire, retracing the evolutionary history of the species. Most interestingly, we have shown that ancient interspecific hybridization events had a major impact in the birth of new variants and therefore in the shaping of the TE repertoires. We also investigated the transpositional activity of these elements in a large set of natural isolates, and we found a broad variability related to the level of ploidy as well as the genetic background. Overall, our results pointed out that the evolution of the Ty content is deeply impacted by clade-specific events such as introgressions and therefore follows the population structure. In addition, our study lays the foundation for future investigations to better understand the transpositional regulation and more broadly the TE-host interactions.

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“…The GRF167 S. cerevisiae strain background utilized in this study is likely “restrictive” for Ty mobilization due to the high copy number of Ty1 elements, and thus, testing transposition rate in interspecific hybrids derived from other “permissive” strain backgrounds is needed. A recent study examining Ty content across natural and experimentally evolved hybrids in the S. paradoxus species complex also found no evidence for increased Ty mobilization in hybrids ( Hénault et al 2020 ). Changes in Ty copy number in some experimentally evolved lines were observed but were not associated with evolutionary divergence between hybrid parents, and instead were highly genotype specific.…”

Section: Discussionmentioning

confidence: 92%

Transposable Element Mobilization in Interspecific Yeast Hybrids

Heil

Patterson

Hickey

et al. 2021

Genome Biology and Evolution

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Barbara McClintock first hypothesized that interspecific hybridization could provide a “genomic shock” that leads to the mobilization of transposable elements. This hypothesis is based on the idea that regulation of transposable element movement is potentially disrupted in hybrids. However, the handful of studies testing this hypothesis have yielded mixed results. Here, we set out to identify if hybridization can increase transposition rate and facilitate colonization of transposable elements in Saccharomyces cerevisiae x Saccharomyces uvarum interspecific yeast hybrids. S. cerevisiae have a small number of active long terminal repeat (LTR) retrotransposons (Ty elements), while their distant relative S. uvarum have lost the Ty elements active in S. cerevisiae. While the regulation system of Ty elements is known in S. cerevisiae, it is unclear how Ty elements are regulated in other Saccharomyces species, and what mechanisms contributed to the loss of most classes of Ty elements in S. uvarum. Therefore, we first assessed whether transposable elements could insert in the S. uvarum sub-genome of a S. cerevisiae x S. uvarum hybrid. We induced transposition to occur in these hybrids and developed a sequencing technique to show that Ty elements insert readily and non-randomly in the S. uvarum genome. We then used an in vivo reporter construct to directly measure transposition rate in hybrids, demonstrating that hybridization itself does not alter rate of mobilization. However, we surprisingly show that species-specific mitochondrial inheritance can change transposition rate by an order of magnitude. Overall, our results provide evidence that hybridization can potentially facilitate the introduction of transposable elements across species boundaries and alter transposition via mitochondrial transmission, but that this does not lead to unrestrained proliferation of transposable elements suggested by the genomic shock theory.

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

Cited by 31 publications

References 128 publications

Heterogeneous mutation rates and spectra in yeast hybrids

Heterogeneous mutation rates and spectra in yeast hybrids

Species-wide transposable element repertoires retrace the evolutionary history of the Saccharomyces cerevisiae host

Transposable Element Mobilization in Interspecific Yeast Hybrids

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