Patterns of piRNA Regulation in <i>Drosophila</i> Revealed through Transposable Element Clade Inference

Said, Iskander; McGurk, Michael P; Clark, Andrew G.; Barbash, Daniel A.

doi:10.1093/molbev/msab336

Cited by 9 publications

(9 citation statements)

References 104 publications

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“…We propose that most G2/Jockey-3 insertions in the centromeres resulted from a burst of activity, which is consistent with the evolutionary history of other non-LTR retroelements [88]. When a TE first invades, it can proliferate rapidly until it comes under the surveillance of germline defense mechanisms like the piRNA pathway for example, by inserting into a piRNA cluster [94][95][96].…”

Section: G2/jockey-3 Copy Number Amplification On the Y Chromosome Is...supporting

confidence: 73%

Centromere-associated retroelement evolution inDrosophila melanogasterreveals an underlying conflict

Hemmer

Negm

Geng

et al. 2022

Preprint

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Centromeres are chromosomal regions essential for coordinating chromosome segregation during cell division. While centromeres are defined by the presence of a centromere-specific histone H3 variant called CENP-A rather than a particular DNA sequence, they are typically embedded in repeat-dense and heterochromatic chromosomal genome regions. In many species, centromeres are associated with transposable elements but it is unclear if these elements are selfish and target centromeres for insertion or if they play a role in centromere specification and function. Here we use Drosophila melanogaster as a model to understand the evolution of centromere-associated transposable elements. G2/Jockey-3 is a non-LTR retroelement in the Jockey clade and the only sequence shared by all centromeres. We study the evolution of G2/Jockey-3 using short and long read population genomic data to infer insertion polymorphisms across the genome. We combine estimates of the age, frequency, and location of insertions to infer the evolutionary processes shaping G2/Jockey-3 and its association with the centromeres. We find that G2/Jockey-3 is an active retroelement that is targeted by the piRNA pathway. Our results suggest that G2-Jockey-3 is highly enriched in centromeres at least in part due to an insertion bias. We do not detect any signature of positive selection on any G2/Jockey-3 insertions that would suggest than individual insertions are favored by natural selection. Instead, we infer that most insertions are neutral or weakly deleterious both inside and outside of the centromeres. Therefore, G2/Jockey-3 evolution is consistent with it being a selfish genetic element that targets centromeres. We suspect targeting centromeres for insertion helps active retroelements like G2/Jockey-3 escape host defenses, as the unique centromeric chromatin may prevent targeting by the host silencing machinery. On the other hand, centromeric TEs insertions may be tolerated or even beneficial if they also contribute to the right transcriptional and chromatin environment. Thus, we suspect centromere-associated retroelements like G2/Jockey-3 reflect a balance between conflict and cooperation at the centromeres.

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Section: G2/jockey-3 Copy Number Amplification On the Y Chromosome Is...supporting

confidence: 73%

Centromere-associated retroelement evolution inDrosophila melanogasterreveals an underlying conflict

Hemmer

Negm

Geng

et al. 2022

Preprint

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“…Transposable elements and the silencing machinery of their hosts are engaged in an arms race in which a novel TE family initially proliferates, the host evolves silencing based on TE sequence identification, and the TE subsequently diverges to evade silencing-or that particular TE remains permanently silenced, but a novel TE invades the host genome and begins the cycle anew (Luo et al, 2020;Zhang et al, 2020;Said et al, 2022;Wei et al, 2022). If balanced by deletion of TE sequences, this arms-race dynamic can be associated with fairly stable genome size over evolutionary timescales, despite turnover in TE content (Kapusta et al, 2017).…”

Section: The Te-silencing Arms Race Dynamic Across Genome Sizesmentioning

confidence: 99%

Transposable element and host silencing activity in gigantic genomes

Wang

Yuan

Tang

et al. 2023

Front. Cell Dev. Biol.

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Transposable elements (TEs) and the silencing machinery of their hosts are engaged in a germline arms-race dynamic that shapes TE accumulation and, therefore, genome size. In animal species with extremely large genomes (>10 Gb), TE accumulation has been pushed to the extreme, prompting the question of whether TE silencing also deviates from typical conditions. To address this question, we characterize TE silencing via two pathways—the piRNA pathway and KRAB-ZFP transcriptional repression—in the male and female gonads of Ranodon sibiricus, a salamander species with a ∼21 Gb genome. We quantify 1) genomic TE diversity, 2) TE expression, and 3) small RNA expression and find a significant relationship between the expression of piRNAs and TEs they target for silencing in both ovaries and testes. We also quantified TE silencing pathway gene expression in R. sibiricus and 14 other vertebrates with genome sizes ranging from 1 to 130 Gb and find no association between pathway expression and genome size. Taken together, our results reveal that the gigantic R. sibiricus genome includes at least 19 putatively active TE superfamilies, all of which are targeted by the piRNA pathway in proportion to their expression levels, suggesting comprehensive piRNA-mediated silencing. Testes have higher TE expression than ovaries, suggesting that they may contribute more to the species’ high genomic TE load. We posit that apparently conflicting interpretations of TE silencing and genomic gigantism in the literature, as well as the absence of a correlation between TE silencing pathway gene expression and genome size, can be reconciled by considering whether the TE community or the host is currently “on the attack” in the arms race dynamic.

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“…Transposable elements and the silencing machinery of their hosts are engaged in an arms race in which a novel TE family initially proliferates, the host evolves silencing based on TE sequence identification, and the TE subsequently diverges to evade silencing ¾ or that particular TE remains permanently silenced, but a novel TE invades the host genome and begins the cycle anew (Luo et al, 2020;Zhang et al, 2020;Said et al, 2022;Wei et al, 2022). If balanced by deletion of TE sequences, this arms-race dynamic can be associated with fairly stable genome size over evolutionary timescales, despite turnover in TE content (Kapusta et al, 2017).…”

Section: The Te-silencing Arms Race Dynamic Across Genome Sizesmentioning

confidence: 99%

Transposable element and host silencing activity in gigantic genomes

Wang

Yuan

Tang

et al. 2022

Preprint

View full text Add to dashboard Cite

Transposable elements (TEs) and the silencing machinery of their hosts are engaged in a germline arms-race dynamic that shapes TE accumulation and, therefore, genome size. In animal species with extremely large genomes (>10 Gb), TE accumulation has been pushed to the extreme, prompting the question of whether TE silencing also deviates from typical conditions. To address this question, we characterize TE silencing via two pathways -- the piRNA pathway and KRAB-ZFP transcriptional repression -- in the male and female gonads of Ranodon sibiricus, a salamander species with a ~21 Gb genome. We quantify 1) genomic TE diversity, 2) TE expression, and 3) small RNA expression and find a significant relationship between the expression of piRNAs and TEs they target for silencing in both sexes. We also quantified TE silencing pathway gene expression in R. sibiricus and 14 other vertebrates with genome sizes ranging from 1 - 130 Gb and find no association between pathway expression and genome size. Taken together, our results reveal that the gigantic R. sibiricus genome includes at least 19 putatively active TE superfamilies, all of which are targeted by the piRNA pathway in proportion to their expression levels, suggesting comprehensive piRNA-mediated silencing. Males have higher TE expression than females, suggesting that they may contribute more to the species' high genomic TE load. We posit that apparently conflicting interpretations of TE silencing and genomic gigantism in the literature, as well as the absence of a correlation between TE silencing pathway gene expression and genome size, can be reconciled by considering whether the TE community or the host is currently on the attack in the arms race dynamic.

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Patterns of piRNA Regulation in Drosophila Revealed through Transposable Element Clade Inference

Cited by 9 publications

References 104 publications

Centromere-associated retroelement evolution inDrosophila melanogasterreveals an underlying conflict

Centromere-associated retroelement evolution inDrosophila melanogasterreveals an underlying conflict

Transposable element and host silencing activity in gigantic genomes

Transposable element and host silencing activity in gigantic genomes

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