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Toxic Y chromosome: increased repeat expression and age-associated heterochromatin loss in male Drosophila with a young Y chromosome

Citation

Nguyen, Alison; Bachtrog, Doris (2021), Toxic Y chromosome: increased repeat expression and age-associated heterochromatin loss in male Drosophila with a young Y chromosome, Dryad, Dataset, https://doi.org/10.6078/D12T4P

Abstract

Sex-specific differences in lifespan are prevalent across the tree of life and influenced by heteromorphic sex chromosomes. In species with XY sex chromosomes, females often outlive males. Males and females can differ in their overall repeat content due to the repetitive Y chromosome, and repeats on the Y might lower survival of the heterogametic sex (toxic Y effect). Here, we take advantage of the well-assembled young Y chromosome of Drosophila miranda to study the sex-specific dynamics of chromatin structure and repeat expression during aging in male and female flies. Male D. miranda have about twice as much repetitive DNA compared to females, and live shorter than females. Heterochromatin is crucial for silencing of repetitive elements, yet old D. miranda flies lose H3K9me3 modifications in their pericentromere, with heterochromatin loss being more severe during aging in males than females. Satellite DNA becomes de-repressed more rapidly in old vs. young male flies relative to females. In contrast to what is observed in D. melanogaster, we find that transposable elements (TEs) are expressed at higher levels in male D. miranda throughout their life. We show that epigenetic silencing via heterochromatin formation is ineffective on the large TE-rich neo-Y chromosome, resulting in up-regulation of Y-linked TEs already in young males. This is consistent with an interaction between the age of the Y chromosome and the genomic effects of aging. Our data support growing evidence that “toxic Y chromosomes” can diminish male fitness and a reduction in heterochromatin can contribute to sex-specific aging.

Methods

Lifespan assays: Flies were collected and aged for the lifespan assay following Linford, N. J., et al. J. Vis. Exp. (2013). We recorded the number of flies dying during multiple aging trials. Data represents fly deaths over time from 4 independent aging trials. Two files are listed - one recording deaths and one recording the remaining alive flies once the experiments stopped.

RNA-Seq: Two data tables are processed with the DESeq2 normalization pipeline. One table contains normalized expression values for transposable elements (TEs) and the other for satellite DNA. The last table shows transposable element expression on a per-chromosome basis from the TECounts/TEtranscripts pipeline. 

ChIP-Seq: Four data tables in total containing H3K9me3 enrichment (ChIP/Input) of different samples/replicates.  One table contains enrichment values for the entire genome of males and females, one table contains values for enrichment at satellite DNA, and two tables contain values for enrichment at TEs (a table containing male data and a table containing female data). 

Usage Notes

Lifespan assay: In both files, the first column indicates the day of the experiment, the second represents females (0) or males (1), and the third represents either alive (1) or dead (2).  These plots combined will yield a survivorship curve.  

ChIP-Seq: Combine the male and female data tables together to view H3K9me3 enrichment at TEs.