The C-Module-Binding Factor Supports Amplification of TRE5-A Retrotransposons in the Dictyostelium discoideum Genome

Bilzer, Annika; Dölz, Heike; Reinhardt, Alexander; Schmith, Anika; Siol, Oliver; Winckler, Thomas

doi:10.1128/ec.00205-10

Cited by 4 publications

(19 citation statements)

References 33 publications

(41 reference statements)

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“…In cells of the CbfA mutant JH.D, both plus-and minus-strand RNA from the retrotransposon TRE5-A is diminished and the mobility of the endogenous retrotransposon population is drastically reduced (13). Thus, CbfA is a positive regulator of TRE5-A amplification.…”

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confidence: 88%

“…Expression and retrotransposition of TRE5-A can be restored in JH.D cells by the ectopic expression of the fulllength CbfA protein. Interestingly, the expression of the isolated carboxy-terminal domain (CTD) of CbfA in the mutant cells was sufficient for complete restoration of the TRE5-A transcript levels, even though TRE5-A retrotransposition was unaffected (13).…”

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confidence: 99%

“…The retrotransposon TRE5-A is characterized by three outstanding features: an active population of elements in the D. discoideum genome is maintained (10), gene disruption rarely occurs because integration is targeted to the vicinity of tRNA genes (11), and a considerable amount of minus strand ("antisense") RNA is produced from a promoter located at the 3= end of the element, the C module (12,13). The large amount of minus strand RNA in growing D. discoideum cells suggests that TRE5-A retrotransposition may be regulated by posttranscriptional silencing.…”

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confidence: 99%

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Conserved Gene Regulatory Function of the Carboxy-Terminal Domain of Dictyostelid C-Module-Binding Factor

Schmith¹,

Groth²,

Ratka³

et al. 2013

Eukaryot Cell

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e C-module-binding factor A (CbfA) is a jumonji-type transcription regulator that is important for maintaining the expression and mobility of the retrotransposable element TRE5-A in the social amoeba Dictyostelium discoideum. CbfA-deficient cells have lost TRE5-A retrotransposition, are impaired in the ability to feed on bacteria, and do not enter multicellular development because of a block in cell aggregation. In this study, we performed Illumina RNA-seq of growing CbfA mutant cells to obtain a list of CbfA-regulated genes. We demonstrate that the carboxy-terminal domain of CbfA alone is sufficient to mediate most CbfAdependent gene expression. The carboxy-terminal domain of CbfA from the distantly related social amoeba Polysphondylium pallidum restored the expression of CbfA-dependent genes in the D. discoideum CbfA mutant, indicating a deep conservation in the gene regulatory function of this domain in the dictyostelid clade. The CbfA-like protein CbfB displays ϳ25% sequence identity with CbfA in the amino-terminal region, which contains a JmjC domain and two zinc finger regions and is thought to mediate chromatin-remodeling activity. In contrast to CbfA proteins, where the carboxy-terminal domains are strictly conserved in all dictyostelids, CbfB proteins have completely unrelated carboxy-terminal domains. Outside the dictyostelid clade, CbfA-like proteins with the CbfA-archetypical JmjC/zinc finger arrangement and individual carboxy-terminal domains are prominent in filamentous fungi but are not found in yeasts, plants, and metazoans. Our data suggest that two functional regions of the CbfAlike proteins evolved at different rates to allow the occurrence of species-specific adaptation processes during genome evolution.

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Conserved Gene Regulatory Function of the Carboxy-Terminal Domain of Dictyostelid C-Module-Binding Factor

Schmith¹,

Groth²,

Ratka³

et al. 2013

Eukaryot Cell

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“…Most likely for the purpose of suppressing transposition, the organism has evolved a sophisticated RNAi machinery that includes, for example, three RNA-dependent RNA polymerases (RdRPs), two Dicer-like proteins, and five Argonaute-like proteins [ 13 – 17 ]. Intriguingly, the non-long terminal repeat retrotransposon TRE5-A has established a fairly high amplification rate in growing D. discoideum cells [ 18 , 19 ] despite the constitutive production of minus-strand RNA from an element-internal promoter [ 20 , 21 ]. Thus, how TRE5-A manipulates the cellular RNAi machinery to maintain its remarkable retrotransposition activity is of interest.…”

Section: Introductionmentioning

confidence: 99%

“…Transcriptome analyses revealed that CbfA has general gene regulatory functions in D. discoideum cells [ 28 ], making this protein an attractive candidate as a host protein that could limit TRE5-A expression and retrotransposition by elevating TRE5-A-derived minus-strand RNA. Interestingly, we observed that both plus- and minus-strand RNA of TRE5-A were reduced concurrently in the CbfA mutant by more than 90 %, and this reduction of transcript levels was accompanied by a sharp drop in TRE5-A’s retrotransposition activity in vivo [ 21 ]. Remarkably, the promoter activity of neither the A-module (TRE5-A’s plus-strand RNA promoter) nor the C-module was altered in reporter gene assays in the CbfA mutant compared to wild-type cells [ 21 ].…”

Section: Introductionmentioning

confidence: 99%

A host factor supports retrotransposition of the TRE5-A population in Dictyostelium cells by suppressing an Argonaute protein

Schmith¹,

Spaller²,

Gaube³

et al. 2015

Mobile DNA

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BackgroundIn the compact and haploid genome of Dictyostelium discoideum control of transposon activity is of particular importance to maintain viability. The non-long terminal repeat retrotransposon TRE5-A amplifies continuously in D. discoideum cells even though it produces considerable amounts of minus-strand (antisense) RNA in the presence of an active RNA interference machinery. Removal of the host-encoded C-module-binding factor (CbfA) from D. discoideum cells resulted in a more than 90 % reduction of both plus- and minus-strand RNA of TRE5-A and a strong decrease of the retrotransposition activity of the cellular TRE5-A population. Transcriptome analysis revealed an approximately 230-fold overexpression of the gene coding for the Argonaute-like protein AgnC in a CbfA-depleted mutant.ResultsThe D. discoideum genome contains orthologs of RNA-dependent RNA polymerases, Dicer-like proteins, and Argonaute proteins that are supposed to represent RNA interference pathways. We analyzed available mutants in these genes for altered expression of TRE5-A. We found that the retrotransposon was overexpressed in mutants lacking the Argonaute proteins AgnC and AgnE. Because the agnC gene is barely expressed in wild-type cells, probably due to repression by CbfA, we employed a new method of promoter-swapping to overexpress agnC in a CbfA-independent manner. In these strains we established an in vivo retrotransposition assay that determines the retrotransposition frequency of the cellular TRE5-A population. We observed that both the TRE5-A steady-state RNA level and retrotransposition rate dropped to less than 10 % of wild-type in the agnC overexpressor strains.ConclusionsThe data suggest that TRE5-A amplification is controlled by a distinct pathway of the Dictyostelium RNA interference machinery that does not require RNA-dependent RNA polymerases but involves AgnC. This control is at least partially overcome by the activity of CbfA, a factor derived from the retrotransposon’s host. This unusual regulation of mobile element activity most likely had a profound effect on genome evolution in D. discoideum.Electronic supplementary materialThe online version of this article (doi:10.1186/s13100-015-0045-5) contains supplementary material, which is available to authorized users.

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The Dictyostelium discoideum RNA-dependent RNA polymerase RrpC silences the centromeric retrotransposon DIRS-1 post-transcriptionally and is required for the spreading of RNA silencing signals

Wiegand¹,

Meier²,

Seehafer³

et al. 2013

Nucleic Acids Research

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Dictyostelium intermediate repeat sequence 1 (DIRS-1) is the founding member of a poorly characterized class of retrotransposable elements that contain inverse long terminal repeats and tyrosine recombinase instead of DDE-type integrase enzymes. In Dictyostelium discoideum, DIRS-1 forms clusters that adopt the function of centromeres, rendering tight retrotransposition control critical to maintaining chromosome integrity. We report that in deletion strains of the RNA-dependent RNA polymerase RrpC, full-length and shorter DIRS-1 messenger RNAs are strongly enriched. Shorter versions of a hitherto unknown long non-coding RNA in DIRS-1 antisense orientation are also enriched in rrpC– strains. Concurrent with the accumulation of long transcripts, the vast majority of small (21 mer) DIRS-1 RNAs vanish in rrpC– strains. RNASeq reveals an asymmetric distribution of the DIRS-1 small RNAs, both along DIRS-1 and with respect to sense and antisense orientation. We show that RrpC is required for post-transcriptional DIRS-1 silencing and also for spreading of RNA silencing signals. Finally, DIRS-1 mis-regulation in the absence of RrpC leads to retrotransposon mobilization. In summary, our data reveal RrpC as a key player in the silencing of centromeric retrotransposon DIRS-1. RrpC acts at the post-transcriptional level and is involved in spreading of RNA silencing signals, both in the 5′ and 3′ directions.

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The C-Module-Binding Factor Supports Amplification of TRE5-A Retrotransposons in the Dictyostelium discoideum Genome

Cited by 4 publications

References 33 publications

Conserved Gene Regulatory Function of the Carboxy-Terminal Domain of Dictyostelid C-Module-Binding Factor

Conserved Gene Regulatory Function of the Carboxy-Terminal Domain of Dictyostelid C-Module-Binding Factor

A host factor supports retrotransposition of the TRE5-A population in Dictyostelium cells by suppressing an Argonaute protein

The Dictyostelium discoideum RNA-dependent RNA polymerase RrpC silences the centromeric retrotransposon DIRS-1 post-transcriptionally and is required for the spreading of RNA silencing signals

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