Establishment of H3K9me3-dependent heterochromatin during embryogenesis in Drosophila miranda

Wei, Kevin H.-C.; Chan, Carolus; Bachtrog, Doris

doi:10.7554/elife.55612

Cited by 31 publications

(24 citation statements)

References 81 publications

(123 reference statements)

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“…An additional role of TEs in the heterochromatin appears to be related to the embryo development. In a recent study, the upstream region of retrotransposons belonging to few active families was identified as the nucleation sites of heterochromatin formation during early stages of embryo development in the fly [ 142 , 143 ], and similar observations have been made in mammals [ 144 ].…”

Section: Te Exaptation In a Heterochromatin-related Contextmentioning

confidence: 82%

Constitutive Heterochromatin in Eukaryotic Genomes: A Mine of Transposable Elements

Marsano

Dimitri

2022

Cells

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Transposable elements (TEs) are abundant components of constitutive heterochromatin of the most diverse evolutionarily distant organisms. TEs enrichment in constitutive heterochromatin was originally described in the model organism Drosophila melanogaster, but it is now considered as a general feature of this peculiar portion of the genomes. The phenomenon of TE enrichment in constitutive heterochromatin has been proposed to be the consequence of a progressive accumulation of transposable elements caused by both reduced recombination and lack of functional genes in constitutive heterochromatin. However, this view does not take into account classical genetics studies and most recent evidence derived by genomic analyses of heterochromatin in Drosophila and other species. In particular, the lack of functional genes does not seem to be any more a general feature of heterochromatin. Sequencing and annotation of Drosophila melanogaster constitutive heterochromatin have shown that this peculiar genomic compartment contains hundreds of transcriptionally active genes, generally larger in size than that of euchromatic ones. Together, these genes occupy a significant fraction of the genomic territory of heterochromatin. Moreover, transposable elements have been suggested to drive the formation of heterochromatin by recruiting HP1 and repressive chromatin marks. In addition, there are several pieces of evidence that transposable elements accumulation in the heterochromatin might be important for centromere and telomere structure. Thus, there may be more complexity to the relationship between transposable elements and constitutive heterochromatin, in that different forces could drive the dynamic of this phenomenon. Among those forces, preferential transposition may be an important factor. In this article, we present an overview of experimental findings showing cases of transposon enrichment into the heterochromatin and their positive evolutionary interactions with an impact to host genomes.

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Section: Te Exaptation In a Heterochromatin-related Contextmentioning

confidence: 82%

Constitutive Heterochromatin in Eukaryotic Genomes: A Mine of Transposable Elements

Marsano

Dimitri

2022

Cells

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“…Further, we find that insertions of TE families with low expression are associated with broader and stronger heterochromatin spreading to their surroundings. Indeed, lowly expressed and high copy number TEs are typically recently active and have robust small RNA targeting for posttranscriptional degradation and transcriptional silencing ( Wei et al 2021 ). Altogether, these results suggest that TE insertions can have multiple effects on gene expression and calls into question how pervasive TE-induced epigenetic silencing of neighboring genes is.…”

Section: Discussionmentioning

confidence: 99%

“…ChIP-seq analyses were slightly modified from methods in Wei et al (2021) . Briefly, larval H3K9me3 ChIP and input data ( Wei and Bachtrog 2019 ) were aligned to the genome using bwa mem.…”

Section: Methodsmentioning

confidence: 99%

Dynamics and Impacts of Transposable Element Proliferation in the Drosophila nasuta Species Group Radiation

Wei

Mai

Chatla

et al. 2022

Molecular Biology and Evolution

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Transposable element (TE) mobilization is a constant threat to genome integrity. Eukaryotic organisms have evolved robust defensive mechanisms to suppress their activity, yet TEs can escape suppression and proliferate, creating strong selective pressure for host defense to adapt. This genomic conflict fuels a never-ending arms race that drives the rapid evolution of TEs and recurrent positive selection of genes involved in host defense; the latter has been shown to contribute to postzygotic hybrid incompatibility. However, how TE proliferation impacts genome and regulatory divergence remains poorly understood. Here, we report the highly complete and contiguous (N50=33.8Mb - 38.0Mb) genome assemblies of seven closely-related Drosophila species that belong to the nasuta species group - a poorly studied group of flies that radiated in the last 2 million years. We constructed a high quality de novo TE library and gathered germline RNA-seq data, which allowed us to comprehensively annotate and compare TE insertion patterns between the species, and infer the evolutionary forces controlling their spread. We find a strong negative association between TE insertion frequency and expression of genes nearby; this likely reflects survivor-bias from reduced fitness impact of TEs inserting near lowly expressed, non-essential genes, with limited TE-induced epigenetic silencing. Phylogenetic analyses of insertions of 147 TE families reveal that 53% of them show recent amplification in at least one species. The most highly amplified TE is a non-autonomous DNA element DINE which has gone through multiple bouts of expansions with thousands of full length copies littered throughout each genome. Across all TEs, we find that TEs expansions are significantly associated with high expression in the expanded species consistent with suppression escape. Thus, while horizontal transfer followed by invasion of a naïve genome has been highlighted to explain the long-term survival of TEs, our analysis suggests that evasion of host suppression of resident TEs is a major strategy to persist over evolutionary times. Altogether, our results shed light on the heterogenous and context-dependent nature in which TEs affect gene regulation and the dynamics of rampant TE proliferation amidst a recently radiated species group.

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“…Further, we find that insertions of TE families with low expression are associated with broader and stronger heterochromatin spreading to their surroundings. Indeed, lowly expressed and high copy number TEs are typically recently active and have robust small RNA targeting for post--transcriptional degradation and transcriptional silencing (Wei et al 2021). Altogether, these results suggest that TE insertions can have multiple effects on gene expression and calls into question how pervasive TE--induced epigenetic silencing of neighboring genes is.…”

Section: Context Dependent Heterochromatin Spreading and Epigenetic Silencingmentioning

confidence: 99%

Dynamics and impacts of transposable element proliferation during the Drosophila nasuta species group radiation

Wei

Mai

Chatla

et al. 2021

Preprint

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Transposable element (TE) mobilization is a constant threat to genome integrity. Eukaryotic organisms have evolved robust defensive mechanisms to suppress their activity, yet TEs can escape suppression and proliferate, creating strong selective pressure for host defense to adapt. This genomic conflict fuels a never-ending arms race that drives the rapid evolution of TEs and recurrent positive selection of genes involved in host defense; the latter has been shown to contribute to postzygotic hybrid incompatibility. However, how TE proliferation impacts genome and regulatory divergence remains poorly understood. Here, we report the highly complete and contiguous (N50=33.8Mb - 38.0Mb) genome assemblies of seven closely-related Drosophila species that belong to the nasuta species group - a poorly studied group of flies that radiated in the last 2 million years. We constructed a high quality de novo TE library and gathered germline RNA-seq data, which allowed us to comprehensively annotate and compare insertion patterns between the species, and infer the evolutionary forces controlling their spread. We find a strong negative association between TE insertion frequency and expression of genes nearby; this likely reflects survivor-bias from reduced fitness impact of TE inserting near lowly expressed, non-essential genes, with limited TE-induced epigenetic silencing. Phylogenetic analyses of insertions of 147 TE families reveal that 53% of them show recent amplification in at least one species. The most highly amplified TE is an non-autonomous DNA element DINE which has gone through multiple bouts of expansions with thousands of full length copies littered throughout each genome. Across all TEs, we find that TEs expansions are significantly associated with high expression in the expanded species consistent with suppression escape. Altogether, our results shed light on the heterogenous and context-dependent nature in which TEs affect gene regulation and the dynamics of rampant TE proliferation amidst a recently radiated species group.

show abstract

Establishment of H3K9me3-dependent heterochromatin during embryogenesis in Drosophila miranda

Cited by 31 publications

References 81 publications

Constitutive Heterochromatin in Eukaryotic Genomes: A Mine of Transposable Elements

Constitutive Heterochromatin in Eukaryotic Genomes: A Mine of Transposable Elements

Dynamics and Impacts of Transposable Element Proliferation in the Drosophila nasuta Species Group Radiation

Dynamics and impacts of transposable element proliferation during the Drosophila nasuta species group radiation

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