Aging in the Drosophila ovary: contrasting changes in the expression of the piRNA machinery and mitochondria but no global release of transposable elements

Erwin, Alexandra A.; Blumenstiel, Justin P.

doi:10.1186/s12864-019-5668-3

Cited by 20 publications

(14 citation statements)

References 89 publications

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“…Selected populations subsequently increased whereas controls decreased expression, meeting at a similar expression level at old age. This is comparable with recent studies which suggested that age-dependent changes in TE expression differ between genotypes ( Erwin and Blumenstiel 2019 ; Everett et al 2020 ).…”

Section: Resultssupporting

confidence: 92%

“…Opposing our hypothesis, two recent studies in termites ( Elsner et al 2018 ) and D. melanogaster ( Erwin and Blumenstiel 2019 ) suggest that the germline is protected from TE invasions through increased transcription of the piRNA machinery. Indeed, our expression analysis confirms that many genes associated with transcriptional and post-transcriptional TE silencing tend to be upregulated with age.…”

Section: Discussioncontrasting

confidence: 79%

“…The list of genes involved in TE regulation consisted of piRNA pathway genes also analyzed in Erwin and Blumenstiel 2019 and Elsner et al 2018 , and genes involved in heterochromatic and chromatin structure from Lee and Karpen 2017 . We further added seven genes involved in these functions, and genes annotated to “regulation of transposition” (GO:0010528) and “transposition” (GO:0032196) according to FlyBase so that we ended up with a total of 96 genes ( supplementary table S14 , Supplementary Material online).…”

Section: Methodsmentioning

confidence: 99%

“…Indeed, research has identified longevity-promoting effects of several genes involved in the RNAi machinery and heterochromatin formation ( Mori et al 2012 ; Wood and Helfand 2013 ; Wood et al 2016 ). Interestingly, it is possible that age-related misexpression of TEs is exclusive to the soma due to efficient post-transcriptional TE silencing mediated by the piRNA machinery in the germline ( Sturm et al 2015 ; Elsner et al 2018 ; Erwin and Blumenstiel 2019 ). Considering current evidence, it seems natural that longevity can be achieved through impeding TE activity and controlling the genomic content of TEs.…”

Section: Introductionmentioning

confidence: 99%

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Transposable Element Landscape in Drosophila Populations Selected for Longevity

Fabian

Dönertaş

Fuentealba

et al. 2021

Genome Biology and Evolution

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Transposable elements (TEs) inflict numerous negative effects on health and fitness as they replicate by integrating into new regions of the host genome. Even though organisms employ powerful mechanisms to demobilize TEs, transposons gradually lose repression during aging. The rising TE activity causes genomic instability and was implicated in age-dependent neurodegenerative diseases, inflammation and the determination of lifespan. It is therefore conceivable that long-lived individuals have improved TE silencing mechanisms resulting in reduced TE expression relative to their shorter-lived counterparts and fewer genomic insertions. Here, we test this hypothesis by performing the first genome-wide analysis of TE insertions and expression in populations of Drosophila melanogaster selected for longevity through late-life reproduction for 50-170 generations from four independent studies. Contrary to our expectation, TE families were generally more abundant in long-lived populations compared to non-selected controls. Although simulations showed that this was not expected under neutrality, we found little evidence for selection driving TE abundance differences. Additional RNA-seq analysis revealed a tendency for reducing TE expression in selected populations, which might be more important for lifespan than regulating genomic insertions. We further find limited evidence of parallel selection on genes related to TE regulation and transposition. However, telomeric TEs were genomically and transcriptionally more abundant in long-lived flies, suggesting improved telomere maintenance as a promising TE-mediated mechanism for prolonging lifespan. Our results provide a novel viewpoint indicating that reproduction at old age increases the opportunity of TEs to be passed on to the next generation with little impact on longevity.

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Section: Resultssupporting

confidence: 92%

Section: Discussioncontrasting

confidence: 79%

Section: Methodsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Transposable Element Landscape in Drosophila Populations Selected for Longevity

Fabian

Dönertaş

Fuentealba

et al. 2021

Genome Biology and Evolution

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“…In line with termite workers, increased TE activity with age occurs in Drosophila somatic tissues [19][20][21], albeit with the caveat that TE insertion rates are prone to overestimation in sequencing data [22]. It has been hypothesised that that age-related misexpression of TEs is restricted to somatic tissues due to continued efficient policing of the germline by the piRNA response with age [17,18,23].…”

Section: Ageing and The Pirna Pathway In Arthropodsmentioning

confidence: 87%

Daphnia magna egg piRNA cluster expression profiles change as mothers age

Hearn

Little

2021

Preprint

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PiRNAs prevent transposable elements wreaking havoc on the germline genome. Changes in piRNA expression over the lifetime of an individual may impact on ageing through continued suppression, or release, of transposable element expression. We identified piRNA producing clusters in the genome of Daphnia magna by a combination of bioinformatic methods, and then contrasted their expression between parthenogenetically produced eggs representing maternally-deposited germline piRNAs of young (having their 1st clutch) and old (having their 5th clutch) mothers. Results from eggs were compared to cluster expression in three generations of adults. As for other arthropods, D. magna encodes long uni-directionally transcribed non-coding RNAs which consist of transposable element fragments which account for most piRNAs expressed. Egg tissues showed extensive differences between clutches from young mothers and those from old mothers, with 578 and 686 piRNA clusters upregulated, respectively, although most log fold-change differences for significant clusters were modest. When considering only highly expressed clusters, there was a bias towards 1st clutch eggs at 41 upregulated versus eight clusters in the eggs from older mothers. F0 generation differences between young and old mothers were fewer than eggs, as 179 clusters were up-regulated in young versus 170 old mothers. This dropped to 31 versus 22 piRNA clusters when comparing adults in the F1 generation, and no differences were detected in the F3 generation. These patterns were similar to that observed for D. magna micro-RNA expression. Little overlap in differentially expressed clusters was found between adults containing mixed somatic and germline (ovary) tissues and germ-line representing eggs. A cluster encompassing a Tudor domain containing gene important in the piRNA pathway was upregulated in the eggs from old mothers. We hypothesise that regulation of this gene this could form part of a feedback loop that reduces piRNA pathway activity explaining the reduced number of highly-expressed clusters in eggs from old mothers.Author SummarySmall RNAs shorter than 200 nucleotides often function by targeting RNAs with complementary nucleotide sequences for destruction. A subset of small RNAs, the Piwi-interacting RNAs or piRNAs are best known for silencing sequences of DNA that can jump between locations in the genome which can compromise the integrity of genomes. This protects offspring from sterility and other undesirable effects, hence piRNAs have been termed ‘guardians of the genome’. PiRNAs have several characteristics, such as a characteristic length and origin in genomic graveyards of junk DNA, that can be used to distinguish them from other small RNAs. Here, we used a combination of computational approaches to identify piRNA-producing clusters in the genome of the water flea Daphnia magna. We then contrasted expression of these clusters between genetically identical adults of different ages, their eggs, adult offspring and great-granddaughters. Adults and their eggs were markedly different in cluster expression by age, which was mostly lost by adulthood in offspring and not seen at all in great-granddaughters. By taking an innovative approach that can be applied to similar datasets of diverse organisms we have shown that piRNA expression, and therefore, stability of the genome can change with age.

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Development of a novel forensic age estimation strategy for aged blood samples by combining piRNA and miRNA markers

Chen

Zhou

et al. 2023

Int J Legal Med

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Aging in the Drosophila ovary: contrasting changes in the expression of the piRNA machinery and mitochondria but no global release of transposable elements

Cited by 20 publications

References 89 publications

Transposable Element Landscape in Drosophila Populations Selected for Longevity

Transposable Element Landscape in Drosophila Populations Selected for Longevity

Daphnia magna egg piRNA cluster expression profiles change as mothers age

Development of a novel forensic age estimation strategy for aged blood samples by combining piRNA and miRNA markers

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