Light and shadow on the mechanisms of integration site selection in yeast Ty retrotransposon families

Bonnet, Amandine; Lesage, Pascale

doi:10.1007/s00294-021-01154-7

Cited by 14 publications

(8 citation statements)

References 115 publications

(130 reference statements)

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“…Multigene families of tDNAs are transcribed by the RNA polymerase III and serve as genomic targets for de novo transposition of the Ty1 to Ty4 elements (Bonnet and Lesage, 2021). As a result, tDNAs are usually located in complex repetitive regions of the chromosomes that cannot be assembled by short read genome sequencing.…”

Section: Dynamics Of Tdnas Multigene Familiesmentioning

confidence: 99%

142 telomere-to-telomere assemblies reveal the genome structural landscape inSaccharomyces cerevisiae

O’Donnell

Saada

Agier

et al. 2022

Preprint

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As population genomics is transitioning from single reference genomes to pangenomes, major improvements in terms of genome contiguity, phylogenetic sampling, haplotype phasing and structural variant (SV) calling are required. Here, we generated the Saccharomyces cerevisiae Reference Assembly Panel (ScRAP) comprising 142 reference-quality genomes from strains of various geographic and ecological origins that faithfully represent the genomic diversity and complexity of the species. The ca. 4,800 independent SVs we identified impact the expression of genes near the breakpoints and contribute to gene repertoire evolution through disruptions, duplications, fusions and horizontal transfers. We discovered frequent cases of complex aneuploidies, preferentially involving large chromosomes that underwent large SVs. We also characterized the evolutionary dynamics of complex genomic regions that classically remain unassembled in short read-based projects, including the 5 Ty families and the 32 individual telomeres. Overall, the ScRAP represents a crucial step towards establishing a high-quality, unified and complete S. cerevisiae pangenome.

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Section: Dynamics Of Tdnas Multigene Familiesmentioning

confidence: 99%

142 telomere-to-telomere assemblies reveal the genome structural landscape inSaccharomyces cerevisiae

O’Donnell

Saada

Agier

et al. 2022

Preprint

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“…Chen et al 2003; Hashida et al 2003; Hashida et al 2006; Sehgal et al 2007; Chenais et al 2012; Jardim et al 2015; Miousse et al 2015; Esnault et al 2019; Fouche et al 2020; Roquis et al 2021), including in Saccharomyces cerevisiae (Bradshaw and McEntee 1989; Wilke and Adams 1992; Scholes et al 2003; Sacerdot et al 2005; Todeschini et al 2005; Servant et al 2008; Stoycheva et al 2010; Servant et al 2012), leading to an increase in transposon-driven mutagenesis. S. cerevisiae has five families of Long Terminal Repeat (LTR) retrotransposons: Ty1 - Ty5 (Rowley 2017; Bonnet and Lesage 2021). Ty1 and Ty2 are closely related and are the two most abundant families in the reference genome.…”

Section: Introductionmentioning

confidence: 99%

Paths to adaptation under fluctuating nitrogen starvation: The spectrum of adaptive mutations in Saccharomyces cerevisiae is shaped by transposons and microhomology-mediated recombination

Hays

Schwartz

Schmidtke

et al. 2022

Preprint

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There are many mechanisms that give rise to genomic change: point mutations are often emphasized in genomic analyses, but evolution acts through many mechanisms that give rise to less subtle perturbations. Changes in chromosome structure, DNA copy number, and novel transposon insertions all create large genomic changes, which can have correspondingly large impacts on phenotypes and fitness. In this study we investigate the spectrum of adaptive mutations that arise in a population under fluctuating nitrogen starvation conditions. We specifically contrast these adaptive alleles and the mutational mechanisms that create them, with mechanisms of adaption under glucose limitation and continuous selection in low, non-fluctuating, nitrogen conditions. We observe that retrotransposon activity accounts for a substantial number of adaptive alleles, along with microhomology-mediated mechanisms of insertion, deletion, and gene conversion. In addition to loss of function alleles, which are often exploited in genetic screens, we identify adaptive gain of function alleles and alleles acting through as-of-yet unclear mechanisms. Taken together our findings emphasize that how selection is applied shapes adaptation, just as the selective pressure does itself. Fluctuating environments can activate different mutational mechanisms, shaping adaptive alleles accordingly. Using experimental evolution is thus a complementary approach to both classical genetic screens and natural variant studies as a way to characterize the genotype-to-phenotype-to-fitness map.

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“…Previously [15], we used the well-established pattern that Ty1, Ty2, Ty3 and Ty4 non-randomly target promoters of genes transcribe by RNA polymerase III such as tRNAs (reviewed in [81]) to validate non-reference TE predictions made by Mc-Clintock 1 component methods in small sample of 93 S. cerevisiae genomes [15, 63]. Here, we confirm that the majority of non-reference predictions made by all component methods in McClintock 2 for these four Ty families are in the expected vicinity of tRNA genes in the species-wide S. cerevisiae resequencing dataset analyzed here (Fig.…”

Section: Resultsmentioning

confidence: 99%

Reproducible evaluation of transposable element detectors with McClintock 2 guides accurate inference of Ty insertion patterns in yeast

Chen

Basting

Han

et al. 2023

Preprint

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Background: Many computational methods have been developed to detect non-reference transposable element (TE) insertions using short-read whole genome sequencing data. The diversity and complexity of such methods often present challenges to new users seeking to reproducibly install, execute or evaluate multiple TE insertion detectors. Results: We previously developed the McClintock meta-pipeline to facilitate the installation, execution, and evaluation of six first-generation short-read TE detectors. Here, we report a completely re-implemented version of McClintock written in Python using Snakemake and Conda that improves its installation, error handling, speed, stability, and extensibility. McClintock 2 now includes 12 short-read TE detectors, auxiliary pre-processing and analysis modules, interactive HTML reports, and a simulation framework to reproducibly evaluate the accuracy of component TE detectors. When applied to the model microbial eukaryote Saccharomyces cerevisiae, we find substantial variation in the ability of McClintock 2 components to identify the precise locations of non-reference TE insertions, with RelocaTE2 showing the highest recall and precision in simulated data. We find that RelocaTE2, TEMP, TEMP2 and TEBreak provide a consistent and biologically meaningful view of non-reference TE insertions in a species-wide panel of ∼1000 yeast genomes, as evaluated by coverage-based abundance estimates and expected patterns of tRNA promoter targeting. Finally, we show that best-in-class predictors for yeast have sufficient resolution to reveal a dyad pattern of integration in nucleosome-bound regions upstream of yeast tRNA genes for Ty1, Ty2, and Ty4, allowing us to extend knowledge about fine-scale target preferences first revealed experimentally for Ty1 to natural insertions and related copia-superfamily retrotransposons in yeast. Conclusion: McClintock (https://github.com/bergmanlab/mcclintock/) provides a user-friendly pipeline for the identification of TEs in short-read WGS data using multiple TE detectors, which should benefit researchers studying TE insertion variation in a wide range of different organisms. Application of the improved McClintock system to simulated and empirical yeast genome data reveals best-in-class methods and novel biological insights for one of the most widely-studied model eukaryotes and provides a paradigm for evaluating and selecting non-reference TE detectors for other species.

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Light and shadow on the mechanisms of integration site selection in yeast Ty retrotransposon families

Cited by 14 publications

References 115 publications

142 telomere-to-telomere assemblies reveal the genome structural landscape inSaccharomyces cerevisiae

142 telomere-to-telomere assemblies reveal the genome structural landscape inSaccharomyces cerevisiae

Paths to adaptation under fluctuating nitrogen starvation: The spectrum of adaptive mutations in Saccharomyces cerevisiae is shaped by transposons and microhomology-mediated recombination

Reproducible evaluation of transposable element detectors with McClintock 2 guides accurate inference of Ty insertion patterns in yeast

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