Maternal enhancement of cytotype regulation inDrosophila melanogasterby genetic interactions between telomericPelements and non-telomeric transgenicPelements

Simmons, Michael; Ragatz, Lisa M.; Sinclair, Ian; Thorp, Michael W.; Buschette, Jared T.; Grimes, Craig D.

doi:10.1017/s0016672312000523

Cited by 10 publications

(17 citation statements)

References 41 publications

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“…Empirical data regarding the quantitative relationship between TE copy numbers inside and outside of piRNA clusters and reductions in transposition rate are sparse for P -elements, and entirely lacking for other TE families. We therefore harnessed the extensive data on piRNAmediated repression of dysgenic sterility (Marin et al, 2000;Ronsseray et al, 1991Ronsseray et al, , 1996Ronsseray et al, , 1998Simmons et al, 2014Simmons et al, , 2007Simmons et al, , 2012Stuart et al, 2002) (Supplemental Material Table S1, figure S1). Based on these observations, we describe the strength of small-RNA-mediated silencing, R, conferred by maternal genotypes with at least one occupied small-RNA site as…”

Section: Small-rna-mediated Silencingmentioning

confidence: 99%

The Evolution of Small-RNA-Mediated Silencing of an Invading Transposable Element

Kelleher

Azevedo

Zheng

2017

Preprint

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Transposable elements (TEs) are genomic parasites that impose fitness costs on their hosts by producing deleterious mutations and disrupting gametogenesis. Host genomes avoid these costs by regulating TE activity, particularly in germline cells where new insertions are heritable and TEs are exceptionally active. However, the capacity of different TE-associated fitness costs to select for repression in the host, and the role of selection in the evolution of TE regulation more generally, remain controversial. In this study, we use individual-based simulations to examine the evolution of TE regulation through small RNA-mediated silencing. Small RNA silencing is a common mechanism for TE regulation employed by both prokaryotes and eukaryotes. We observed that even under conservative assumptions, where small RNA-mediated regulation reduces transposition only, repression evolves rapidly and adaptively after the genome is invaded by a new TE. We further show that the spread of repressor alleles is greatly enhanced by two additional TE-imposed fitness costs: dysgenic sterility and ectopic recombination. Finally, we demonstrate that the mutation rate to repression (i.e., the size of the mutational target) is a critical parameter that influences both the evolutionary trajectory of host repression and the associated proliferation of TEs. Our findings suggest that adaptive evolution of TE regulation may be stronger and more prevalent than previously suggested, and complement recent empirical observations of positive selection on small RNA-mediated repressor alleles. Both prokaryotic and eukaryotic genomes minimize the fitness costs of TEs by controlling their activity through small RNA mediated silencing (reviewed in Blumenstiel 2011). In eukaryotic germlines, small RNA mediated silencing of TEs is enacted by Argonaute proteins that are found in complex with small interfering RNAs (siRNAs) and Piwi-interacting RNAs (piRNAs). Regulatory siRNAs and piRNAs are produced from anti-sense TE transcripts, and identify TE-derived mRNAs by base complementarity. Complexed Argonaute proteins then silence the targeted TE transcriptionally by inducing heterochromatin formation, or post-transcriptionally by degrading the transcript. Consistent with prevention of germline DNA damage, small RNA-mediated silencing suppresses TE-associated dysgenic sterility in Drosophila (Blumenstiel and Hartl 2005;Brennecke et al. 2008;Chambeyron et al. 2008;Rozhkov et al.

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Section: Small-rna-mediated Silencingmentioning

confidence: 99%

The Evolution of Small-RNA-Mediated Silencing of an Invading Transposable Element

Kelleher

Azevedo

Zheng

2017

Preprint

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“…Therefore, mRNAs from nonrepressive P insertions would enhance piRNA production that is initiated by insertions in the X-TAS piRNA cluster, thereby establishing stronger regulation. In support of this model, aub mutations impair both ping-pong amplification ) and the enhanced repression exhibited by maternal genotypes combining TPs with nonrepressive P insertions (Belinco et al 2009;Simmons et al 2012Simmons et al , 2014.…”

Section: P Cytotype Is Established By P-element Insertions In Pirna Cmentioning

confidence: 81%

“…However, significantly-stronger maternal repression is seen when the maternal genotype includes both a TP and additional P elements elsewhere in the genome ( Figure 5B vs. Figure 5C) (Ronsseray et al 1998;Simmons et al 2007aSimmons et al , 2012Simmons et al , 2014Belinco et al 2009). TP-dependent maternal repression, therefore, is epistatically enhanced by additional P-element copies, which in isolation do not confer repression.…”

Section: P Cytotype Is Established By P-element Insertions In Pirna Cmentioning

confidence: 99%

Reexamining the P-Element Invasion of Drosophila melanogaster Through the Lens of piRNA Silencing

Kelleher¹

2016

Genetics

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Transposable elements (TEs) are both important drivers of genome evolution and genetic parasites with potentially dramatic consequences for host fitness. The recent explosion of research on regulatory RNAs reveals that small RNA-mediated silencing is a conserved genetic mechanism through which hosts repress TE activity. The invasion of the Drosophila melanogaster genome by P elements, which happened on a historical timescale, represents an incomparable opportunity to understand how small RNAmediated silencing of TEs evolves. Repression of P-element transposition emerged almost concurrently with its invasion. Recent studies suggest that this repression is implemented in part, and perhaps predominantly, by the Piwi-interacting RNA (piRNA) pathway, a small RNA-mediated silencing pathway that regulates TE activity in many metazoan germlines. In this review, I consider the P-element invasion from both a molecular and evolutionary genetic perspective, reconciling classic studies of P-element regulation with the new mechanistic framework provided by the piRNA pathway. I further explore the utility of the P-element invasion as an exemplar of the evolution of piRNA-mediated silencing. In light of the highly-conserved role for piRNAs in regulating TEs, discoveries from this system have taxonomically broad implications for the evolution of repression.

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“…This is because the vast majority of TART piRNAs in the protective mothers are derived from the tip of the X chromosome from 160 (Figure 7C) and three of the six females that are most protective against dysgenesis lack the X 160 telomere allele. Notably, the telomeric region of the X has special silencing properties in D. melanogaster that may explain the excess of TART piRNAs derived from this one genomic region [45,46,47,48,49], but in this system this region plays no role in protection against dysgenesis.…”

Section: Resultsmentioning

confidence: 99%

When genomes collide: multiple modes of germline misregulation in a dysgenic syndrome ofDrosophila virilis

et al. 2014

Preprint

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1 2In sexually reproducing species the union of gametes that are not closely related 3 can result in genomic incompatibility. Hybrid dysgenic syndromes represent a 4 form of genomic incompatibility that can arise when transposable element (TE) 5 abundance differs between two parents. When TEs lacking in the female parent 6 are transmitted paternally, a lack of corresponding silencing small RNAs 7 (piRNAs) transmitted through the female germline can lead to TE mobilization in 8 progeny. The epigenetic nature of this phenomenon is demonstrated by the fact 9 that genetically identical females of the reciprocal cross are normal. Here we 10show that in the hybrid dysgenic syndrome of Drosophila virilis, an excess of 11 paternally inherited TE families leads not only to increased expression of these 12TEs, but also coincides with derepression of TEs in equal abundance within 13 parents. Moreover, TE derepression is stable as flies age and associated with 14 piRNA biogenesis defects for only some TEs. At the same time, TE activation is 15 associated with a genome wide shift in the distribution of endogenous gene 16 expression and an increase in abundance of off-target genic piRNAs. To identify 17 regions of the maternal genome that most protect against dysgenesis, we 18 performed an F3 backcross analysis. We find that pericentric regions play a 19 dominant role in maternal protection. This F3 backcross approach additionally 20 allowed us to clarify the properties of genic paramutation in D. virilis. Overall, 21 results support a model in which early germline events in dysgenesis establish a 22 chronic, stable state of mis-expression that is maintained through adulthood. 23

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Maternal enhancement of cytotype regulation inDrosophila melanogasterby genetic interactions between telomericPelements and non-telomeric transgenicPelements

Cited by 10 publications

References 41 publications

The Evolution of Small-RNA-Mediated Silencing of an Invading Transposable Element

The Evolution of Small-RNA-Mediated Silencing of an Invading Transposable Element

Reexamining the P-Element Invasion of Drosophila melanogaster Through the Lens of piRNA Silencing

When genomes collide: multiple modes of germline misregulation in a dysgenic syndrome ofDrosophila virilis

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