Retrotransposons and Their Recognition of pol II Promoters: A Comprehensive Survey of the Transposable Elements From the Complete Genome Sequence of Schizosaccharomyces pombe

Abstract

The complete DNA sequence of the genome of Schizosaccharomyces pombe provides the opportunity to investigate the entire complement of transposable elements (TEs), their association with specific sequences, their chromosomal distribution, and their evolution. Using homology-based sequence identification, we found that the sequenced strain of S. pombe contained only one family of full-length transposons. This family, Tf2, consisted of 13 full-length copies of a long terminal repeat (LTR) retrotransposon. We found that LTR-LTR recombination of previously existing transposons had resulted in extensive populations of solo LTRs. These included 35 solo LTRs of Tf2, as well as 139 solo LTRs from other Tf families. Phylogenetic analysis of solo Tf LTRs reveals that Tf1 and Tf2 were the most recently active elements within the genome. The solo LTRs also served as footprints for previous insertion events by the Tf retrotransposons. Analysis of 186 genomic insertion events revealed a close association with RNA polymerase II promoters. These insertions clustered in the promoter-proximal regions of genes, upstream of protein coding regions by 100 to 400 nucleotides. The association of Tf insertions with pol II promoters was very similar to the preference previously observed for Tf1 integration. We found that the recently active Tf elements were absent from centromeres and pericentromeric regions of the genome containing tandem tRNA gene clusters. In addition, our analysis revealed that chromosome III has twice the density of insertion events compared to the other two chromosomes. Finally we describe a novel repetitive sequence, wtf, which was also preferentially located on chromosome III, and was often located near solo LTRs of Tf elements.

The Spontaneous Mutation Rate in the Fission Yeast Schizosaccharomyces pombe

“…The left and right breakpoints of the shorter event are within the highly similar repeat elements wtf19 and wtf21 (Bowen et al 2003), and the breakpoints of the longer event are within highly similar LTR Tf2 elements. Despite being haploid, S. pombe undergoes an extended G 2 phase of the cell cycle, presenting an opportunity for unequal crossover between sister chromatids, a likely mechanism for such large duplications.…”

Mapping genomic hotspots of DNA damage by a single-strand-DNA-compatible and strand-specific ChIP-seq method

“…5A). Tf2 belongs to the Ty3/Gypsy family of long terminal repeat (LTR)-containing retrotransposons and is the only type of transposable elements capable of remobilization in standard S. pombe strains (Bowen et al 2003). ChIP-enriched reads can also be aligned to the Tf-fragment 1 element, and a number of solo LTRs, probably due to their sequence similarity to the full-length Tf2.…”

Single-Nucleotide-Specific Targeting of the Tf1 Retrotransposon Promoted by the DNA-Binding Protein Sap1 of Schizosaccharomyces pombe

“…In Schizosaccharomyces pombe, the LTR retrotransposon Tf1 has a unique targeting mechanism that directs integration to promoters of RNA polymerase II-transcribed genes with a bias for the promoters of stress-response genes (Behrens et al 2000;Singleton and Levin 2002;Bowen et al 2003;Leem et al 2008;Guo and Levin 2010). Surprisingly, insertion of Tf1 into promoters rarely reduces the expression of their downstream genes, and in approximately 40% of cases, it enhances it (Feng et al 2013).…”

“…The ability of these elements to selectively integrate into specific target sequences has been paramount to their success because the employment of specific targeting mechanisms has allowed these retrotransposons to propagate within host genomes without disrupting genes and compromising the host's survival (Levin and Moran 2011). The long terminal repeat (LTR) retrotransposons Ty1, Ty3, and Ty5 of Saccharomyces cerevisiae avoid causing damage to the host by targeting noncoding genomic regions; Ty1 and Ty3 integrate upstream of RNA polemerase III-transcribed genes, while Ty5 integrates into heterochromatin (Chalker and Sandmeyer 1990;1992;Ji et al 1993;Kirchner et al 1995;Devine and Boeke 1996;Zou et al 1996;Zou and Voytas 1997;Yieh et al 2000;Sandmeyer 2003;Lesage and Todeschini 2005).In Schizosaccharomyces pombe, the LTR retrotransposon Tf1 has a unique targeting mechanism that directs integration to promoters of RNA polymerase II-transcribed genes with a bias for the promoters of stress-response genes (Behrens et al 2000;Singleton and Levin 2002;Bowen et al 2003;Leem et al 2008;Guo and Levin 2010). Surprisingly, insertion of Tf1 into promoters rarely reduces the expression of their downstream genes, and in approximately 40% of cases, it enhances it (Feng et al 2013).…”