Antisense Transcription of Retrotransposons in <i>Drosophila</i>: An Origin of Endogenous Small Interfering RNA Precursors

Russo, Joseph; Harrington, Andrew W.; Steiniger, Mindy

doi:10.1534/genetics.115.177196

Cited by 27 publications

(45 citation statements)

References 77 publications

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“…Rodriguez and I. R. Arkhipova processed into piRNAs (Shpiz et al 2014). Even TEs inserted in the same orientation have the potential to promote aberrant transcription due to widespread presence of antisense promoters (Russo et al 2015). While A. vaga harbors many extended genomic regions enriched in TEs that yield sRNA coverage over large distances, thereby resembling extended piRNA clusters in other species, a significant share of piRNA production also comes from much smaller regions where it apparently can be acquired on a gene-by-gene basis.…”

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confidence: 99%

Multitasking of the piRNA Silencing Machinery: Targeting Transposable Elements and Foreign Genes in the Bdelloid Rotifer Adineta vaga

Rodríguez¹,

Arkhipova

2016

Genetics

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RNA-mediated silencing processes play a key role in silencing of transposable elements, especially in the germ line, where piwiinteracting RNAs (piRNAs) are responsible for suppressing transposon mobility and maintaining genome integrity. We previously reported that the genome of Adineta vaga, the first sequenced representative of the phylum Rotifera (class Bdelloidea), is characterized by massive levels of horizontal gene transfer, by unusually low transposon content, and by highly diversified RNA-mediated silencing machinery. Here, we investigate genome-wide distribution of pi-like small RNAs, which in A. vaga are 25-31 nucleotides in length and have a strong 59-uridine bias, while lacking ping-pong amplification signatures. In agreement with expectations, 71% of mapped reads corresponded to annotated transposons, with 93% of these reads being in the antisense orientation. Unexpectedly, a significant fraction of piRNAs originate from predicted coding regions corresponding to genes of putatively foreign origin. The distribution of piRNAs across foreign genes is not biased toward 39-UTRs, instead resembling transposons in uniform distribution pattern throughout the gene body, and in predominantly antisense orientation. We also find that genes with small RNA coverage, including a number of genes of metazoan origin, are characterized by higher occurrence of telomeric repeats in the surrounding genomic regions, and by higher density of transposons in the vicinity, which have the potential to promote antisense transcription. Our findings highlight the complex interplay between RNA-based silencing processes and acquisition of genes at the genome periphery, which can result either in their loss or eventual domestication and integration into the host genome.KEYWORDS piwi-interacting RNAs; horizontal gene transfer; mobile genetic elements; telomeres B DELLOID rotifers are common invertebrate animals a few tenths of a millimeter long, primarily found in fresh water, temporary pools, and other ephemerally aquatic habitats (Ricci and Melone 2000). Class Bdelloidea is classified in four families and 19 genera, with .460 described species (Segers 2007) in which there is no evidence of sex or meiosis in their life cycle, suggesting completely asexual reproduction (Mark Welch et al. 2008;Flot et al. 2013). The class, characterized by their ciliated head and bilateral ovaries, is known to have an ancient origin: bdelloid remains have been identified in 35-to 40-million-year-old amber, and the substantial number of synonymous site substitutions indicates that different bdelloid families have diverged tens of millions of years ago (Poinar and Ricci 1992;Mark Welch et al. 2008). They are able to survive in ephemerally aquatic environments due to their ability to withstand desiccation and subsequently resume reproduction at any stage of their life cycle. Bdelloids can also resist high doses of ionizing radiation, probably as a result of adaptation to their desiccation-prone life style. A dose as high as 500 Gy can cause DN...

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confidence: 99%

Multitasking of the piRNA Silencing Machinery: Targeting Transposable Elements and Foreign Genes in the Bdelloid Rotifer Adineta vaga

Rodríguez¹,

Arkhipova

2016

Genetics

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“…33 These elements were chosen for further investigation as S and AS transcription of these Tns was observed previously. 15 We conclude that while a few AS RNA-seq reads are observed for these TIR Tns, very few esiRNAs are generated from these transcripts indicating that TIR Tn movement is minimally regulated by esiRNAs in Drosophila melanogaster somatic cells. Additionally, we discovered that unlike retroTns, few individual TIR Tns are transcribed in either the S or AS direction.…”

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confidence: 73%

“…Examination of length distributions for previously investigated non-LTR retrotransposons (retroTns) Juan and Jockey and LTR retroTns blood, mdg1 and 297 revealed a much higher percentage of full-length elements than observed for pogo and 1360 (data not shown). 15 The variability of Note. The percent (% total) of 1360 and pogo TIR Tns in each size class is shown in the left three columns.…”

Section: Resultsmentioning

confidence: 99%

“…To investigate S and AS pogo and 1360 Tn transcription and potential esiRNA biogenesis, small RNA-seq and RNA-seq data sets from control Drosophila tissue culture (Dmel-2) cells 15 were mapped to the Drosophila genome followed by visualization of non-unique and unique reads using the UCSC genome browser (http:// genome.ucsc.edu, Dm6 assembly, August 2014). 36,37 Examples of representative full-length intergenic pogo and 1360 elements show RNA-seq reads mapping to both S and AS strands, although the number of normalized AS reads (reads per million (RPM)) is low ( Fig.…”

Section: As Tir Tn Transcripts Are Not Produced From Intraelement Tssmentioning

confidence: 99%

“…Drosophila melanogaster has several classes of both retroTns and TIR Tns, 1 although retroTns appear to be more active. 3,15 Movement of both retroTns and TIR Tns must be regulated to ensure genomic stability. In Drosophila, 2 non-coding RNA mediated post-transcriptional silencing mechanisms have been elucidated.…”

Section: Introductionmentioning

confidence: 99%

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Bioinformatic analyses of sense and antisense expression from terminal inverted repeat transposons inDrosophilasomatic cells

Harrington

Steiniger

2016

Fly

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Understanding regulation of transposon movement in somatic cells is important as mobile elements can cause detrimental genomic rearrangements. Generally, transposons move via one of 2 mechanisms; retrotransposons utilize an RNA intermediate, therefore copying themselves and amplifying throughout the genome, while terminal inverted repeat transposons (TIR Tns) excise DNA sequences from the genome and integrate into a new location. Our recently published work indicates that retrotransposons in Drosophila tissue culture cells are actively transcribed in the antisense direction. Our data support a model in which convergent transcription of retrotransposons from intra element transcription start sites results in complementary RNAs that hybridize to form substrates for Dicer-2, the endogenous small interfering (esi)RNA generating enzyme. Here, we extend our previous analysis to TIR Tns. In contrast to retrotransposons, our data show that antisense TIR Tn RNAs result from transcription of intronic TIR Tns oriented antisense to their host genes. Also, disproportionately less esiRNAs are generated from TIR transcripts than from retrotransposons and transcription of very few individual TIR Tns could be confirmed. Collectively, these data support a model in which TIR Tns are regulated at the level of Transposase production while retrotransposons are regulated with esiRNA post-transcriptional mechanisms in Drosophila somatic cells.

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Transposable elements: Self‐seekers of the germline, team‐players of the soma

Haig

2016

BioEssays

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The germ track is the cellular path by which genes are transmitted to future generations whereas somatic cells die with their body and do not leave direct descendants. Transposable elements (TEs) evolve to be silent in somatic cells but active in the germ track. Thus, the performance of most bodily functions by a sequestered soma reduces organismal costs of TEs. Flexible forms of gene regulation are permissible in the soma because of the self-imposed silence of TEs, but strict licensing of transcription and translation is maintained in the germ track to control proliferation of TEs. Delayed zygotic genome activation (ZGA) and maternally inherited germ granules are adaptations that enhance germ-track security. Mammalian embryos exhibit very early ZGA associated with extensive mobilization of retroelements. This window of vulnerability to retrotransposition in early embryos is an indirect consequence of evolutionary conflicts within the mammalian genome over postzygotic maternal provisioning.

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Antisense Transcription of Retrotransposons in Drosophila: An Origin of Endogenous Small Interfering RNA Precursors

Cited by 27 publications

References 77 publications

Multitasking of the piRNA Silencing Machinery: Targeting Transposable Elements and Foreign Genes in the Bdelloid Rotifer Adineta vaga

Multitasking of the piRNA Silencing Machinery: Targeting Transposable Elements and Foreign Genes in the Bdelloid Rotifer Adineta vaga

Bioinformatic analyses of sense and antisense expression from terminal inverted repeat transposons inDrosophilasomatic cells

Transposable elements: Self‐seekers of the germline, team‐players of the soma

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