Reactivation of transposable elements following hybridization in fission yeast

Hybridization is thought to reactivate transposable elements (TEs) that were efficiently suppressed in the genomes of the parental hosts. Here, we provide evidence for this 'genomic shock hypothesis' in the fission yeast Schizosaccharomyces pombe. The species is characterized by divergence of two ancestral lineages (Sp and Sk) which have experienced recent, likely human induced, hybridization. We used long-read sequencing data to assemble genomes of 37 samples derived from 31 S. pombe strains spanning a wide range of ancestral admixture proportions. A comprehensive TE inventory revealed exclusive presence of long terminal repeat (LTR) retrotransposons. In-depth sequence analyses of active full-length elements, as well as solo-LTRs, revealed a complex history of homologous recombination. Population genetic analyses of syntenic sequences placed insertion of many solo-LTRs prior to the split of the Sp and Sk lineages. Most full-length elements were inserted more recently after hybridization. With the exception of a single full-length element with signs of positive selection, both solo-LTRs, and in particular, full-length elements carried signatures of purifying selection indicating effective removal by the host. Consistent with reactivation upon hybridization, the number of full-length LTR retrotransposons, varying extensively from zero to 87 among strains, significantly increased with the degree of genomic admixture. This study gives a detailed account of global TE diversity in S. pombe, documents complex recombination histories within TE elements and provides evidence for the ‘genomic shock hypothesis’ with implications for the role of TEs in adaptation and speciation.

Reactivation of transposable elements following hybridization in fission yeast

Hybridization is thought to reactivate transposable elements (TEs) that were efficiently suppressed in the genomes of the parental hosts. Here, we provide evidence for this 'genomic shock hypothesis' in the fission yeast Schizosaccharomyces pombe. The species is characterized by divergence of two ancestral lineages (Sp and Sk) which have experienced recent, likely human induced, hybridization. We used long-read sequencing data to assemble genomes of 37 samples derived from 31 S. pombe strains spanning a wide range of ancestral admixture proportions. A comprehensive TE inventory revealed exclusive presence of long terminal repeat (LTR) retrotransposons. In-depth sequence analyses of active full-length elements, as well as solo-LTRs, revealed a complex history of homologous recombination. Population genetic analyses of syntenic sequences placed insertion of many solo-LTRs prior to the split of the Sp and Sk lineages. Most full-length elements were inserted more recently after hybridization. With the exception of a single full-length element with signs of positive selection, both solo-LTRs, and in particular, full-length elements carried signatures of purifying selection indicating effective removal by the host. Consistent with reactivation upon hybridization, the number of full-length LTR retrotransposons, varying extensively from zero to 87 among strains, significantly increased with the degree of genomic admixture. This study provides a detailed account of global TE diversity in S. pombe, documents complex recombination histories within TE elements and provides first evidence for the 'genomic shock hypothesis' in fungi with implications for the role of TEs in adaptation and speciation.

Asymmetric Somatic Hybridization Affects Synonymous Codon Usage Bias in Wheat

Asymmetric somatic hybridization is an efficient strategy for crop breeding by introducing exogenous chromatin fragments, which leads to whole genomic shock and local chromosomal shock that induces genome-wide genetic variation including indel (insertion and deletion) and nucleotide substitution. Nucleotide substitution causes synonymous codon usage bias (SCUB), an indicator of genomic mutation and natural selection. However, how asymmetric somatic hybridization affects SCUB has not been addressed. Here, we explored this issue by comparing expressed sequence tags of a common wheat cultivar and its asymmetric somatic hybrid line. Asymmetric somatic hybridization affected SCUB and promoted the bias to A- and T-ending synonymous codon (SCs). SCUB frequencies in chromosomes introgressed with exogenous fragments were comparable to those in chromosomes without exogenous fragments, showing that exogenous fragments had no local chromosomal effect. Asymmetric somatic hybridization affected SCUB frequencies in indel-flanking sequences more strongly than in non-flanking sequences, and this stronger effect was present in both chromosomes with and without exogenous fragments. DNA methylation-driven SCUB shift was more pronounced than other SC pairs. SCUB shift was similar among seven groups of allelic chromosomes as well as three sub-genomes. Our work demonstrates that the SCUB shift induced by asymmetric somatic hybridization is attributed to the whole genomic shock, and DNA methylation is a putative force of SCUB shift during asymmetric somatic hybridization. Asymmetric somatic hybridization provides an available method for deepening the nature of SCUB shift and genetic variation induced by genomic shock.

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.

Robustness of Transposable Element regulation but no genomic shock observed in interspecific Arabidopsis hybrids

The merging of two divergent genomes in a hybrid is believed to trigger a “genomic shock”, disrupting gene regulation and transposable element (TE) silencing. Here, we tested this expectation by comparing the pattern of expression of transposable elements in their native and hybrid genomic context. For this, we sequenced the transcriptome of the Arabidopsis thaliana genotype Col-0, the A. lyrata genotype MN47 and their F1 hybrid. Contrary to expectations, we observe that the level of TE expression in the hybrid is strongly correlated to levels in the parental species. We detect that at most 1.1% of expressed transposable elements belonging to two specific subfamilies change their expression level upon hybridization. Most of these changes, however, are of small magnitude. We observe that the few hybrid-specific modifications in TE expression are more likely to occur when TE insertions are close to genes. In addition, changes in epigenetic histone marks H3K9me2 and H3K27me3 following hybridization do not coincide with TEs with changed expression. Finally, we further examined TE expression in parents and hybrids exposed to severe dehydration stress. Despite the major reorganization of gene and TE expression by stress, we observe that hybridization does not lead to increased disorganization of TE expression in the hybrid. We conclude that TE expression is globally robust to hybridization and that the term “genomic shock” is no longerappropriate to describe the anticipated consequences of merging divergent genomes in a hybrid.