Active retrotransposons help maintain pericentromeric heterochromatin required for faithful cell division

Wang, Dongpeng; Wu, Shuheng; Li, Xiao; Shao, Chunli; Zhang, Peng; Chen, Jia Yu; Lim, Do Hwan; Fu, Xiang-Dong; Chen, Runsheng; He, Shunmin

doi:10.1101/gr.256131.119

Cited by 10 publications

(8 citation statements)

References 47 publications

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“…Indeed, work in Arabidopsis revealed R-loop dynamics were not strongly associated with RNA abundance (Xu et al 2020). Recently, using the newly elucidated global DNA:RNA interaction sequencing (GRID-seq), Hao and colleagues reported that various active retrotransposons, especially those from the gypsy family of the LTR class, produced a large amount of repeat RNAs with the ability to act in both cis and trans on chromatin to help maintain pericentromeric heterochromatin (Hao et al 2020). In maize, retrotransposons were major components of pericentromeric heterochromatin, and we found that the majority of R-loops were derived from LTR/Gypsy and LTR/Copia families (Supplemental Table S1).…”

Section: Discussionmentioning

confidence: 99%

Genome-wide mapping reveals R-loops associated with centromeric repeats in maize

Liu

et al. 2021

Genome Res.

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R-loops are stable chromatin structures comprising a DNA:RNA hybrid and a displaced single-stranded DNA. R-loops have been implicated in gene expression and chromatin structure, as well as in replication blocks and genome instability. Here, we conducted a genome-wide identification of R-loops and identified more than 700,000 R-loop peaks in the maize (Zea mays) genome. We found that sense R-loops were mainly enriched in promoters and transcription termination sites and relatively less enriched in gene bodies, which is different from the main gene-body localization of sense R-loops in Arabidopsis and Oryza sativa. At the chromosome scale, maize R-loops were enriched in pericentromeric heterochromatin regions, and a significant portion of R-loops were derived from transposable elements. In centromeres, R-loops preferentially formed within the binding regions of the centromere-specific histone CENH3, and centromeric retrotransposons were strongly associated with R-loop formation. Furthermore, centromeric retrotransposon R-loops were observed by applying the single-molecule imaging technique of atomic force microscopy. These findings elucidate the fundamental character of R-loops in the maize genome and reveal the potential role of R-loops in centromeres.

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Section: Discussionmentioning

confidence: 99%

Genome-wide mapping reveals R-loops associated with centromeric repeats in maize

Liu

et al. 2021

Genome Res.

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“…The co-localization of LINE-1 RNA and Smarcad1 in the heterochromatin regions is Kap1-dependent and enriches with H3K9me3 loci in mESCs. We suggest that LINE-1 RNAs may be involved in the heterochromatin organization in the form of Smarcad1-LINE1-Kap1 in mouse, similar to the function of ERV RNAs (Hao et al 2020;Liu et al 2021).…”

Section: Discussionmentioning

confidence: 80%

“…Recent studies have highlighted the benefits of transposon RNAs to 3D genome structure, chromatin accessibility and heterochromatin formation (Jachowicz et al 2017; Hao et al 2020; Liu et al 2020; Lu et al 2021). In particular, the advanced high-throughput experimental biotechnologies exploring RNA-chromatin interactions are enabling the deep understanding of the potential function of transposon RNAs on DNA regulation in cells.…”

Section: Discussionmentioning

confidence: 99%

“…These highthroughput experimental data provide a special opportunity for us to explore the interactions between transposon-derived RNAs and chromatin for the understanding of the potential trans-regulatory function of these transposon RNAs. Researchers initiated to utilize the RNA-chromatin interaction data for the discovery that transposon RNAs modulate the process of heterochromatin organization (Hao et al 2020;Chen et al 2021;Liu et al 2021). In this study, we performed a high-throughput proximity MARGI experiment in E14 cells and interpreted the roles of transposon RNAs from the perspective of RNA trans-regulation on gene transcription in embryonic stem cells (ESCs).…”

Section: Introductionmentioning

confidence: 99%

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Chromatin-interacting transposon RNAs linking to the core trans-inhibition circuitry for embryonic stem cell identity

Ren

Zheng

2021

Preprint

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Transposable DNA sequences constitute more than half of the human and mouse genomes. A large number of non-coding RNAs, named as transposon RNAs, are derived from these transposable elements. The cis-regulatory function of transposable DNA elements, such as LINE-1 and Alu has been largely explored. But the biological roles of transposon RNAs aren't well understood. Here, investigations of RNA-chromatin interactions provide us with comprehensive evidence that specific families of transposon RNAs play roles in trans-regulation linking to the core inhibition circuitry for embryonic stem cell identity. Alternative modes of the RNA-DNA hybrid duplex and protein-recruited RNA scaffold are required for the regulatory activities of transposon RNAs. LINE-1 RNAs co-locating with KAP1 form a negative feedback loop stabilizing the transcription of LINE-1 DNA elements via RNA-DNA hybrids. In another way LINE-1 RNAs, together with the reprogramming three factors and Polycomb repressive complexes, participate in the inhibition on dozens of differentiation-relative genes.

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“…Likewise, Drosophila centromeres are TE-rich [53,54], and processing of retrotransposon transcripts into siRNAs is required to maintain pericentromeric heterochromatin [55]. Thus in the utilisation of RNAi as a primary mechanism to regulate TEs, the centromeric clustering of these mobile elements, and their use as a platform for assembly of critical heterochromatin, S. japonicus has much in common with plants and animals, establishing it as an attractive model in which to study both RNAi and centromere function.…”

Section: Discussionmentioning

confidence: 99%

Separable roles for RNAi in regulation of transposable elements and viability in the fission yeast Schizosaccharomyces japonicus

Chapman

Taglini

Bayne

2022

Preprint

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RNA interference (RNAi) is a conserved mechanism of small RNA-mediated genome regulation commonly involved in suppression of transposable elements (TEs) through both post-transcriptional silencing, and transcriptional repression via heterochromatin assembly. The fission yeast Schizosaccharomyces pombe has been extensively utilised as a model for studying RNAi pathways. However, this species is somewhat atypical in that TEs are not major targets of RNAi, and instead small RNAs correspond primarily to non-coding pericentromeric repeat sequences, reflecting a specialised role for the pathway in promoting heterochromatin assembly in these regions. In contrast, in the related fission yeast Schizosaccharomyces japonicus, sequenced small RNAs correspond primarily to TEs. This suggests there may be fundamental differences in the operation of RNAi pathways in these two related species. To investigate these differences, we probed RNAi function in S. japonicus. Unexpectedly, and in contrast to S. pombe, we found that RNAi is essential in this species. Moreover, viability of RNAi mutants can be rescued by mutations implicated in enhanching RNAi-independent heterochromatin propagation. These rescued strains retain heterochromatic marks on TE sequences, but exhibit derepression of TEs at the post-transcriptional level. Our findings indicate that S. japonicus retains the ancestral role of RNAi in facilitating suppression of TEs via both post-transcriptional silencing and heterochromatin assembly, with specifically the heterochromatin pathway being essential for viability, likely due to a function in genome maintenance. The specialised role of RNAi in heterochromatin assembly in S. pombe appears to be a derived state that emerged after the divergence of S. japonicus.

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Active retrotransposons help maintain pericentromeric heterochromatin required for faithful cell division

Cited by 10 publications

References 47 publications

Genome-wide mapping reveals R-loops associated with centromeric repeats in maize

Genome-wide mapping reveals R-loops associated with centromeric repeats in maize

Chromatin-interacting transposon RNAs linking to the core trans-inhibition circuitry for embryonic stem cell identity

Separable roles for RNAi in regulation of transposable elements and viability in the fission yeast Schizosaccharomyces japonicus

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