Evolutionary dynamics between transposable elements and their host genomes: mechanisms of suppression and escape

Lawlor, Matthew A; Ellison, Christopher E

doi:10.1016/j.gde.2023.102092

Cited by 7 publications

(4 citation statements)

References 80 publications

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“…Our examination of evolution in coding regions flagged germ cell-specific piRNA factors, as well as some pleiotropic piRNA processing associated complexes (EJC outer shell, EJC transient factors, NSL complex, SUMO modifiers, and Nuclear CBC) as under positive selection. This is unsurprising in the case of primary piRNA processing factors in the germline, as there are many examples of these factors being under selection [ 52 – 60 ]. For instance, replacement of D. melanogaster rhino and deadlock genes with D. simulans homologues results in non-functionality [ 53 ].…”

Section: Discussionmentioning

confidence: 99%

Rapid evolution of promoters from germline-specifically expressed genes including transposon silencing factors

McQuarrie,

Alizada,

Nicholson

et al. 2024

BMC Genomics

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Background The piRNA pathway in animal gonads functions as an ‘RNA-based immune system’, serving to silence transposable elements and prevent inheritance of novel invaders. In Drosophila, this pathway relies on three gonad-specific Argonaute proteins (Argonaute-3, Aubergine and Piwi) that associate with 23–28 nucleotide piRNAs, directing the silencing of transposon-derived transcripts. Transposons constitute a primary driver of genome evolution, yet the evolution of piRNA pathway factors has not received in-depth exploration. Specifically, channel nuclear pore proteins, which impact piRNA processing, exhibit regions of rapid evolution in their promoters. Consequently, the question arises whether such a mode of evolution is a general feature of transposon silencing pathways. Results By employing genomic analysis of coding and promoter regions within genes that function in transposon silencing in Drosophila, we demonstrate that the promoters of germ cell-specific piRNA factors are undergoing rapid evolution. Our findings indicate that rapid promoter evolution is a common trait among piRNA factors engaged in germline silencing across insect species, potentially contributing to gene expression divergence in closely related taxa. Furthermore, we observe that the promoters of genes exclusively expressed in germ cells generally exhibit rapid evolution, with some divergence in gene expression. Conclusion Our results suggest that increased germline promoter evolution, in partnership with other factors, could contribute to transposon silencing and evolution of species through differential expression of genes driven by invading transposons.

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Section: Discussionmentioning

confidence: 99%

Rapid evolution of promoters from germline-specifically expressed genes including transposon silencing factors

McQuarrie,

Alizada,

Nicholson

et al. 2024

BMC Genomics

View full text Add to dashboard Cite

show abstract

“…Our examination of evolution in coding regions flagged germ cell-specific piRNA factors, as well as some pleiotropic piRNA processing associated complexes (EJC outer shell, EJC transient facts, NSL complex, SUMO modifiers, and Nuclear CBC) as under positive selection. This is unsurprising in the case of primary piRNA processing factors in the germline, as there are many examples of these factors being under selection [48–56]. For instance, replacement of D. melanogaster rhino and deadlock genes with D. simulans homologues results in non-functionality [49].…”

Section: Discussionmentioning

confidence: 99%

Rapid evolution of promoters from germline-specifically expressed genes including transposon silencing factors

McQuarrie,

Alizada,

Czech Nicholson

et al. 2023

Preprint

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BackgroundThe piRNA pathway in animal gonads functions as an ‘RNA-based immune system’, serving to silence transposable elements and prevent inheritance of novel invaders. InDrosophila, this pathway relies on three gonad-specific Argonaute proteins (Argonaute-3, Aubergine and Piwi) that associate with 23-28 nucleotide piRNAs, directing the silencing of transposon-derived transcripts. Transposons constitute a primary driver of genome evolution, yet the evolution of piRNA pathway factors has not received in-depth exploration. Specifically, channel nuclear pore proteins, which impact piRNA processing, exhibit regions of rapid evolution in their promoters. Consequently, the question arises whether such a mode of evolution is a general feature of transposon silencing pathways.ResultsBy employing phylogenomic analysis of coding and promoter regions within genes that function in transposon silencing inDrosophila, we demonstrate that the promoters of germ cell-specific piRNA factors are undergoing rapid evolution. Our findings indicate that rapid promoter evolution is a common trait among piRNA factors engaged in germline silencing across insect species, potentially contributing to gene expression divergence in closely related taxa. Furthermore, we observe that the promoters of genes exclusively expressed in germ cells generally exhibit rapid evolution, which correlates with divergent gene expression.ConclusionsOur results suggest that promoter evolution could have wide impact on transposon silencing and evolution of species through differential expression of genes driven by invading transposons.

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“…Host TE silencing pathways function to curb the harmful effects of TE proliferation, and hosts and TEs show patterns of sequence evolution consistent with coevolution between two entities that are in conflict, akin to an antagonistic host/parasite dynamic (Luo, et al 2020;Lawlor and Ellison 2023). After a novel TE invades a genome, or alternatively after a TE evolves in sequence to escape host silencing, pressure is put on the host to curb that TE's activity.…”

Section: Introductionmentioning

confidence: 96%

“…Transposable elements (TEs) are a diverse group of parasitic sequences that replicate and spread throughout host genomes using a variety of mechanisms, all of which include transcription (Wicker, et al 2007;Lawlor and Ellison 2023). Found in all eukaryotes, their activity is suppressed by several host transcriptional and post-transcriptional silencing pathways (Czech and Hannon 2016;Deniz, et al 2019;Almeida, et al 2022).…”

Section: Introductionmentioning

confidence: 99%

Size evolution of gigantic genomes suggests stochastic outcomes of transposable element/host silencing interactions

Wang,

Zhang,

Sun

et al. 2024

Preprint

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Size evolution among gigantic genomes involves gain and loss of many gigabases of transposable elements (TEs), sequences that parasitize host genomes. Animals suppress TEs using piRNA and KRAB-ZFP pathways. TEs and hosts coevolve in an arms race, where suppression strength reflects TE fitness costs. In enormous genomes, additional TE costs become miniscule. How, then, do TEs and host suppression invoke further addition of massive DNA amounts? We analyzed TE proliferation histories, deletion rates, and community diversities in six salamander genomes (21.3 - 49.9 Gb), alongside gonadal expression of TEs and suppression pathways. TE activity is higher in testes than ovaries, attributable to lower KRAB-ZFP suppression. Unexpectedly, genome size/expansion is uncorrelated with TE deletion rate, proliferation history, expression, and host suppression. Also, TE community diversity increases with genome size, contrasting theoretical predictions. TE/host antagonism in gigantic genomes likely produces stochastic TE accumulation, determined by noisy intermolecular interactions in huge genomes/cells.

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Evolutionary dynamics between transposable elements and their host genomes: mechanisms of suppression and escape

Cited by 7 publications

References 80 publications

Rapid evolution of promoters from germline-specifically expressed genes including transposon silencing factors

Rapid evolution of promoters from germline-specifically expressed genes including transposon silencing factors

Rapid evolution of promoters from germline-specifically expressed genes including transposon silencing factors

Size evolution of gigantic genomes suggests stochastic outcomes of transposable element/host silencing interactions

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