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Transposable elements (TEs) and the silencing machinery of their hosts are engaged in a germline arms-race dynamic that shapes TE accumulation and, therefore, genome size. In animal species with extremely large genomes (>10 Gb), TE accumulation has been pushed to the extreme, prompting the question of whether TE silencing also deviates from typical conditions. To address this question, we characterize TE silencing via two pathways—the piRNA pathway and KRAB-ZFP transcriptional repression—in the male and female gonads of Ranodon sibiricus , a salamander species with a ∼21 Gb genome. We quantify 1) genomic TE diversity, 2) TE expression, and 3) small RNA expression and find a significant relationship between the expression of piRNAs and TEs they target for silencing in both ovaries and testes. We also quantified TE silencing pathway gene expression in R. sibiricus and 14 other vertebrates with genome sizes ranging from 1 to 130 Gb and find no association between pathway expression and genome size. Taken together, our results reveal that the gigantic R. sibiricus genome includes at least 19 putatively active TE superfamilies, all of which are targeted by the piRNA pathway in proportion to their expression levels, suggesting comprehensive piRNA-mediated silencing. Testes have higher TE expression than ovaries, suggesting that they may contribute more to the species’ high genomic TE load. We posit that apparently conflicting interpretations of TE silencing and genomic gigantism in the literature, as well as the absence of a correlation between TE silencing pathway gene expression and genome size, can be reconciled by considering whether the TE community or the host is currently “on the attack” in the arms race dynamic.
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TE Density: a tool to investigate the biology of transposable elements
Abstract Background Transposable elements (TEs) are powerful creators of genotypic and phenotypic diversity due to their inherent mutagenic capabilities and in this way they serve as a deep reservoir of sequences for genomic variation. As agents of genetic disruption, a TE’s potential to impact phenotype is partially a factor of its location in the genome. Previous research has shown TEs’ ability to impact the expression of neighboring genes, however our understanding of this trend is hampered by the exceptional amount of diversity in the TE world, and a lack of publicly available computational methods that quantify the presence of TEs relative to genes. Results Here, we have developed a tool to more easily quantify TE presence relative to genes through the use of only a gene and TE annotation, yielding a new metric we call TE Density. Briefly defined as the proportion of TE-occupied base-pairs relative to a window-size of the genome. This new pipeline reports TE density for each gene in the genome, for each type descriptor of TE (order and superfamily), and for multiple positions and distances relative to the gene (upstream, intragenic, and downstream) over sliding, user-defined windows. In this way, we overcome previous limitations to the study of TE-gene relationships by focusing on all TE types present in the genome, utilizing flexible genomic distances for measurement, and reporting a TE presence metric for every gene in the genome. Conclusions Together, this new tool opens up new avenues for studying TE-gene relationships, genome architecture, comparative genomics, and the tremendous diversity present of the TE world. TE Density is open-source and freely available at: https://github.com/sjteresi/TE_Density .
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- Award ID(s):
- 2029959
- PAR ID:
- 10380818
- Date Published:
- Journal Name:
- Mobile DNA
- Volume:
- 13
- Issue:
- 1
- ISSN:
- 1759-8753
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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Abstract Transposable elements (TEs) are a major determinant of eukaryotic genome size. The collective properties of a genomic TE community reveal the history of TE/host evolutionary dynamics and impact present-day host structure and function, from genome to organism levels. In rare cases, TE community/genome size has greatly expanded in animals, associated with increased cell size and changes to anatomy and physiology. Here, we characterize the TE landscape of the genome and transcriptome in an amphibian with a giant genome — the caecilianIchthyophis bannanicus, which we show has a genome size of 12.2 Gb. Amphibians are an important model system because the clade includes independent cases of genomic gigantism. The I. bannanicus genome differs compositionally from other giant amphibian genomes, but shares a low rate of ectopic recombination-mediated deletion. We examine TE activity using expression and divergence plots; TEs account for 15% of somatic transcription, and most superfamilies appear active. We quantify TE diversity in the caecilian, as well as other vertebrates with a range of genome sizes, using diversity indices commonly applied in community ecology. We synthesize previous models that integrate TE abundance, diversity, and activity, and test whether the caecilian meets model predictions for genomes with high TE abundance. We propose thorough, consistent characterization of TEs to strengthen future comparative analyses. Such analyses will ultimately be required to reveal whether the divergent TE assemblages found across convergent gigantic genomes reflect fundamental shared features of TE/host genome evolutionary dynamics.more » « less
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Bomblies, K (Ed.)Abstract Transposable elements (TEs) have the potential to create regulatory variation both through the disruption of existing DNA regulatory elements and through the creation of novel DNA regulatory elements. In a species with a large genome, such as maize, many TEs interspersed with genes create opportunities for significant allelic variation due to TE presence/absence polymorphisms among individuals. We used information on putative regulatory elements in combination with knowledge about TE polymorphisms in maize to identify TE insertions that interrupt existing accessible chromatin regions (ACRs) in B73 as well as examples of polymorphic TEs that contain ACRs among four inbred lines of maize including B73, Mo17, W22, and PH207. The TE insertions in three other assembled maize genomes (Mo17, W22, or PH207) that interrupt ACRs that are present in the B73 genome can trigger changes to the chromatin, suggesting the potential for both genetic and epigenetic influences of these insertions. Nearly 20% of the ACRs located over 2 kb from the nearest gene are located within an annotated TE. These are regions of unmethylated DNA that show evidence for functional importance similar to ACRs that are not present within TEs. Using a large panel of maize genotypes, we tested if there is an association between the presence of TE insertions that interrupt, or carry, an ACR and the expression of nearby genes. While most TE polymorphisms are not associated with expression for nearby genes, the TEs that carry ACRs exhibit enrichment for being associated with higher expression of nearby genes, suggesting that these TEs may contribute novel regulatory elements. These analyses highlight the potential for a subset of TEs to rewire transcriptional responses in eukaryotic genomes.more » « less
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Lerat, Emmanuelle (Ed.)Abstract Methylated CHH (mCHH) islands are peaks of CHH methylation that occur primarily upstream to genes. These regions are actively targeted by the methylation machinery, occur at boundaries between heterochromatin and euchromatin, and tend to be near highly expressed genes. Here we took an evolutionary perspective by studying upstream mCHH islands across a sample of eight grass species. Using a statistical approach to define mCHH islands as regions that differ from genome-wide background CHH methylation levels, we demonstrated that mCHH islands are common and associate with 39% of genes, on average. We hypothesized that islands should be more frequent in genomes of large size, because they have more heterochromatin and hence more need for defined boundaries. We found, however, that smaller genomes tended to have a higher proportion of genes associated with 5′ mCHH islands. Consistent with previous work suggesting that islands reflect the silencing of the edge of transposable elements (TEs), genes with nearby TEs were more likely to have mCHH islands. However, the presence of mCHH islands was not a function solely of TEs, both because the underlying sequences of islands were often not homologous to TEs and because genic properties also predicted the presence of 5′ mCHH islands. These genic properties included length and gene-body methylation (gbM); in fact, in three of eight species, the absence of gbM was a stronger predictor of a 5′ mCHH island than TE proximity. In contrast, gene expression level was a positive but weak predictor of the presence of an island. Finally, we assessed whether mCHH islands were evolutionarily conserved by focusing on a set of 2,720 orthologs across the eight species. They were generally not conserved across evolutionary time. Overall, our data establish additional genic properties that are associated with mCHH islands and suggest that they are not just a consequence of the TE silencing machinery.more » « less
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- Free Publicly Accessible Full Text
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Accepted Manuscript1.0
- Journal Article:
- https://doi.org/10.1186/s13100-022-00264-4
