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

Abstract

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.

Evolutionary Dynamics of the Repeatome Explains Contrasting Differences in Genome Sizes and Hybrid and Polyploid Origins of Grass Loliinae Lineages

“…In contrast, other plant groups have experienced the opposite trend, with high-level polyploids exhibiting a drastic reduction in genome size and a considerable shrinkage of their repeatome relative to that of their diploid and low-level polyploid relatives (Chen, 2007;Parisod et al, 2010). The removal of the repetitive elements from the genome, attributed to several recombination mechanisms, and the driven forces that balance the expansions and contractions of the repeatome are still poorly known (Fedoroff, 2012;Drouin et al, 2021). In some exhaustively studied plants (Gossypium, Brachypodium) the abundance of some retrotransposon families and their apparent facility to proliferate (e.g., centromeric transposons) are interpreted as causing increased genome size, while the ability of other families to recombine and lose repeats are considered potential mechanisms for maintaining reduced genome size (Chen et al, 2020;Stritt et al, 2020).…”

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

“…The repetitive nature of TEs makes the full sequence-level resolution of their genomic distribution notoriously difficult ( Goerner-Potvin and Bourque, 2018 ). As such, studies investigating the TE reactivation hypothesis in hybrids have used a variety of methods for quantifying the activity of TEs at different levels, for instance, in terms of genomic abundance ( O’Neill et al, 1998 ; Ungerer et al, 2006 ) or expression level ( Dion-Côté et al, 2014 ; Renaut et al, 2014 ; Drouin et al, 2021 ). Not all methods enable the decomposition of TE load at the level of sequence-resolved insertion loci ( Tusso et al, 2022 ), which is an especially challenging task in heterozygous genomes.…”

“…However, this level of mechanistic understanding is not often matched in other systems. The reactivation hypothesis remained untested in fungi until recent works in budding yeasts of the genus Saccharomyces and in the fission yeast Schizosaccharomyces pombe ( Drouin et al, 2021 ; Hénault et al, 2020 ; Smukowski Heil et al, 2021 ; Tusso et al, 2022 ).…”

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

“…However, this level of mechanistic understanding is not often matched in other systems. The reactivation hypothesis remained untested in fungi until recent works in budding yeasts of the genus Saccharomyces and in the fission yeast Schizosaccharomyces pombe (Drouin et al, 2021; Hénault et al, 2020; Smukowski Heil et al, 2021; Tusso et al, 2021).…”