The Drosophila Y Chromosome Affects Heterochromatin Integrity Genome-Wide.

Emily J Brown,Doris Bachtrog,Alison H Nguyen,John Parsch

doi:10.1093/molbev/msaa082

Emily J Brown, Doris Bachtrog + Show 2 more

Open Access

https://doi.org/10.1093/molbev/msaa082

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Abstract

The Drosophila Y chromosome is gene poor and mainly consists of silenced, repetitive DNA. Nonetheless, the Y influences expression of hundreds of genes genome-wide, possibly by sequestering key components of the heterochromatin machinery away from other positions in the genome. To test the influence of the Y chromosome on the genome-wide chromatin landscape, we assayed the genomic distribution of histone modifications associated with gene activation (H3K4me3) or heterochromatin (H3K9me2 and H3K9me3) in fruit flies with varying sex chromosome complements (X0, XY, and XYY males; XX and XXY females). Consistent with the general deficiency of active chromatin modifications on the Y, we find that Y gene dose has little influence on the genomic distribution of H3K4me3. In contrast, both the presence and the number of Y chromosomes strongly influence genome-wide enrichment patterns of repressive chromatin modifications. Highly repetitive regions such as the pericentromeres, the dot, and the Y chromosome (if present) are enriched for heterochromatic modifications in wildtype males and females, and even more strongly in X0 flies. In contrast, the additional Y chromosome in XYY males and XXY females diminishes the heterochromatic signal in these normally silenced, repeat-rich regions, which is accompanied by an increase in expression of Y-linked repeats. We find hundreds of genes that are expressed differentially between individuals with aberrant sex chromosome karyotypes, many of which also show sex-biased expression in wildtype Drosophila. Thus, Y chromosomes influence heterochromatin integrity genome-wide, and differences in the chromatin landscape of males and females may also contribute to sex-biased gene expression and sexual dimorphisms.

Highlights

The Drosophila Y is a degenerated, heterochromatic chromosome with only a few functional genes, primarily specialized in male reproductive function (Gatti and Pimpinelli 1983; Carvalho et al 2000, 2001; Carvalho 2002)
Fly Strains To compare the chromatin landscape between Drosophila that differ in their sex chromosome karyotype and their amount of repetitive DNA, we set up replicate crosses between D. melanogaster stock number 2549 from the Bloomington Stock Center, which has a compound reversed
We found a gradient of heterochromatic sequence content per diploid cell for the five karyotypes, with X0 males ($109 Mb) < XX females ($125 Mb) < XY males ($148 Mb) < XXY females ($158 Mb) < XYY males ($185 Mb)

Summary

Introduction

The Drosophila Y is a degenerated, heterochromatic chromosome with only a few functional genes, primarily specialized in male reproductive function (Gatti and Pimpinelli 1983; Carvalho et al 2000, 2001; Carvalho 2002). Protein-coding genes from the D. melanogaster Y chromosome are only expressed in germ cells of males, but the effects on global gene expression by different Y chromosomes occur in XXY females and somatic cells of XY males (Lemos et al 2008, 2010; Sackton et al 2011).

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