Control of Telomere Length in Drosophila

Shpiz, Sergey; Kalmykova, Alla

doi:10.5772/38160

Cited by 5 publications

(4 citation statements)

References 120 publications

(201 reference statements)

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“…Coordinating telomere elongation to prevent either complete erosion or overextension is a feature of more typical telomerase-based systems [24,25], and mutational studies suggest that Drosophila has recruited the piRNA and heterochromatin maintenance pathways typically involved in TE suppression into this role [26]. Host factors that interact with the telomeres, such as the capping proteins that assemble onto them and the subtelomeric sequence which directly abut them, may have also evolved properties that regulate HTT activity [27].…”

Section: Introductionmentioning

confidence: 99%

“…One simple means of increasing in copy number is for the HTT to escape regulation by the host genome, and thus conflict between the HTTs and genome (or among the HTTs) is an ever present possibility. Indeed, like their feral cousins, studies using mutations in HTT regulators suggest that they are capable of taking over given the opportunity [26]. Similar to the rapid evolution of the Drosophila HTTs [22,28], some telomereassociated proteins show high evolutionary rates and signatures of positive selection [27,29].…”

Section: Introductionmentioning

confidence: 99%

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Rapid evolution at the Drosophila telomere: transposable element dynamics at an intrinsically unstable locus

McGurk

Dion-Côté

Barbash

2019

Preprint

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Background: Drosophila telomeres have been maintained by three families of active transposable elements (TEs), HeT-A, TAHRE and TART, collectively referred to as HTTs, for tens of millions of years.The conservation of this arrangement contrasts with an unusually high degree of HTT interspecific variation. While the impacts of conflict and domestication are often invoked to explain HTT variation, the telomeres are unstable structures such that neutral mutational processes and evolutionary tradeoffs may also drive HTT evolution. Results:We leveraged population genomic data to analyze nearly 10,000 HTT insertions in 85 D.melanogaster genomes and compared their variation to TE families evolving under more typical dynamics. We find that distinct aspects of HTT copy number variation and sequence diversity largely reflect telomere instability, with HTT insertions being lost at much higher rates than other TEs elsewhere in the genome. However, occasional copy number expansions of both HTTs and other TE families occur, highlighting that the HTTs are, like their feral cousins, typically repressed but primed to take over given the opportunity. We further find that some HTT families may be activated by the erosion of whole telomeres, suggesting the existence of HTT-specific host control mechanisms. Conclusions:Even the persistent telomere localization of HTTs may not reflect domestication, but rather a highly successful evolutionary strategy to reduce their impact on the host genome. We propose that HTT evolution is driven by multiple processes including domestication, genetic conflict, niche specialization, and telomere instability, with the latter two being previously underappreciated and likely predominant.

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Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Rapid evolution at the Drosophila telomere: transposable element dynamics at an intrinsically unstable locus

McGurk

Dion-Côté

Barbash

2019

Preprint

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mentioning

confidence: 99%

A Pooled Sequencing Approach Identifies a Candidate Meiotic Driver inDrosophila

et al. 2017

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Meiotic drive occurs when a selfish element increases its transmission frequency above the Mendelian ratio by hijacking the asymmetric divisions of female meiosis. Meiotic drive causes genomic conflict and potentially has a major impact on genome evolution, but only a few drive loci of large effect have been described. New methods to reliably detect meiotic drive are therefore needed, particularly for discovering moderate-strength drivers that are likely to be more prevalent in natural populations than strong drivers. Here, we report an efficient method that uses sequencing of large pools of backcross (BC1) progeny to test for deviations from Mendelian segregation genome-wide with single-nucleotide polymorphisms (SNPs) that distinguish the parental strains. We show that meiotic drive can be detected by a characteristic pattern of decay in distortion of SNP frequencies, caused by recombination unlinking the driver from distal loci. We further show that control crosses allow allele-frequency distortion caused by meiotic drive to be distinguished from distortion resulting from developmental effects. We used this approach to test whether chromosomes with extreme telomere-length differences segregate at Mendelian ratios, as telomeric regions are a potential hotspot for meiotic drive due to their roles in meiotic segregation and multiple observations of high rates of telomere sequence evolution. Using four different pairings of long and short telomere strains, we find no evidence that extreme telomere-length variation causes meiotic drive in However, we identify one candidate meiotic driver in a centromere-linked region that shows an ∼8% increase in transmission frequency, corresponding to a ∼54:46 segregation ratio. Our results show that candidate meiotic drivers of moderate strength can be readily detected and localized in pools of BC1 progeny.

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“…As with some centromere proteins, multiple proteins involved in telomere regulation in Drosophila show elevated rates of evolution including the telomere cap proteins Hoap and HipHop, multiple genes in the piRNA pathway, and transposable element (TE) repressors like Lhr and Hmr (Schmid and Tautz 1997;Gao et al 2010;Lee and Langley 2010;Blumenstiel 2011;Raffa et al 2011;Satyaki et al 2014;Lee et al in press). As mutant alleles of several of these genes produce long telomeres (Khurana et al 2010;Shpiz et al 2012;Satyaki et al 2014), it raises the possibility that telomere length variation causes meiotic drive, with telomere proteins recurrently evolving to counter telomere lengthening To test this hypothesis, here we sample telomere length variation from a natural population of D. melanogaster, focusing on the most abundant telomeric TE, HeT-A. We report the discovery of unprecedented variation in telomere length, which provides the material to test whether pairing of extreme telomere length variants in a heterozygous female causes meiotic drive.…”

Section: Introductionmentioning

confidence: 99%

A pooled sequencing approach identifies a candidate meiotic driver in Drosophila

Wei

Reddy

Rathnam

et al. 2017

Preprint

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Meiotic drive occurs when a selfish element increases its transmission frequency above the Mendelian ratio by hijacking the asymmetric divisions of female meiosis. Meiotic drive causes genomic conflict and potentially has a major impact on genome evolution, but only a few drive loci of large effect have been described. New methods to reliably detect meiotic drive are therefore needed, particularly for discovering moderate-strength drivers that are likely to be more prevalent in natural populations than strong drivers.Here we report an efficient method that uses sequencing of large pools of backcross (BC1) progeny to test for deviations from Mendelian segregation genome-wide of single-nucleotide polymorphisms (SNPs) that distinguish the parental strains. We show that meiotic drive can be detected by a characteristic pattern of decay in distortion of SNP frequencies, caused by recombination unlinking the driver from distal loci. We further show that control crosses allow allele-frequency distortion caused by meiotic drive to be distinguished from distortion resulting from developmental effects. We used this approach to test whether chromosomes with extreme telomere-length differences segregate at Mendelian ratios, as telomeric regions are a potential hotspot for meiotic drive due to their roles in meiotic segregation and multiple observations of high rates of telomere sequence evolution. Using four different pairings of long and short telomere strains, we find no evidence that extreme telomere-length variation causes meiotic drive in Drosophila. However, we identify one candidate meiotic driver in a centromere-linked region that shows an ~8% increase in transmission frequency, corresponding to a ~54:46 segregation ratio. Our results show that candidate meiotic drivers of moderate strength can be readily detected and localized in pools of F1 progeny.

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Control of Telomere Length in Drosophila

Cited by 5 publications

References 120 publications

Rapid evolution at the Drosophila telomere: transposable element dynamics at an intrinsically unstable locus

Rapid evolution at the Drosophila telomere: transposable element dynamics at an intrinsically unstable locus

A Pooled Sequencing Approach Identifies a Candidate Meiotic Driver inDrosophila

A pooled sequencing approach identifies a candidate meiotic driver in Drosophila

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