Testing the Genomic Shock Hypothesis Using Transposable Element Expression in Yeast Hybrids

Transposable element (TE) insertions are a source of structural variation and can cause genetic instability and gene expression changes. A host can limit the spread of TEs with various repression mechanisms. Many examples of plant and animal interspecific hybrids show disrupted TE repression leading to TE propagation. Recent studies in yeast did not find any increase in transposition rate in hybrids. However, this does not rule out the possibility that the transcriptional or translational activity of TEs increases following hybridization because of a disruption of the host TE control mechanisms. Thus, whether total expression of a TE family is higher in hybrids than in their parental species remains to be examined. We leveraged publically available RNA-seq and ribosomal profiling data on yeast artificial hybrids of the Saccharomyces genus and performed differential expression analysis of their LTR retrotransposons (Ty elements). Our analyses of total mRNA levels show that Ty elements are generally not differentially expressed in hybrids, even when the hybrids are exposed to a low temperature stress condition. Overall, only 2/26 Ty families show significantly higher expression in the S. cerevisiae × S. uvarum hybrids while there are 3/26 showing significantly lower expression in the S. cerevisiae x S. paradoxus hybrids. Our analysis of ribosome profiling data of S. cerevisiae × S. paradoxus hybrids shows similar translation efficiency of Ty in both parents and hybrids, except for Ty1_cer showing higher translation efficiency. Overall, our results do not support the hypothesis that hybridization could act as a systematic trigger of TE expression in yeast and suggest that the impact of hybridization on TE activity is strain and TE specific.

Transposable element mobilization in interspecific yeast hybrids

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.

Transposable element mobilization in interspecific yeast hybrids

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 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.

Whole genome sequencing,de novoassembly and phenotypic profiling for the new budding yeast speciesSaccharomyces jurei

Saccharomyces sensu strictocomplex consist of yeast species, which are not only important in the fermentation industry but are also model systems for genomic and ecological analysis. Here, we present the complete genome assemblies ofSaccharomyces jurei,a newly discoveredSaccharomyces sensu strictospecies from high altitude oaks. Phylogenetic and phenotypic analysis revealed thatS. jureiis a sister-species toS. mikatae,thanS. cerevisiae,andS. paradoxus.The karyotype ofS. jureipresents two reciprocal chromosomal translocations between chromosome VI/VII and I/XIII when compared toS. cerevisiaegenome. Interestingly, while the rearrangement I/XIII is unique toS. jurei,the other is in common withS. mikataestrain IFO1815, suggesting shared evolutionary history of this species after the split betweenS. cerevisiaeandS. mikatae.The number of Ty elements differed in the new species, with a higher number of Ty elements present inS. jureithan inS. cerevisiae.Phenotypically, theS. jureistrain NCYC 3962 has relatively higher fitness than the other strain NCYC 3947Tunder most of the environmental stress conditions tested and showed remarkably increased fitness in higher concentration of acetic acid compared to the othersensu strictospecies. Both strains were found to be better adapted to lower temperatures compared toS. cerevisiae.