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Ancestral Chromatin Configuration Constrains Chromatin Evolution on Differentiating Sex Chromosomes in Drosophila.

Zhou Q, Bachtrog D - PLoS Genet. (2015)

Bottom Line: We show that the neo-sex chromosomes formed <1 million years ago, but nearly 60% of neo-Y linked genes have already become non-functional.Expression levels are generally lower for the neo-Y alleles relative to their neo-X homologs, and the silencing heterochromatin mark H3K9me2, but not H3K9me3, is significantly enriched on silenced neo-Y genes.Yet, neo-X genes are transcriptionally more active in males, relative to females, suggesting the evolution of incipient dosage compensation on the neo-X.

View Article: PubMed Central - PubMed

Affiliation: Department of Integrative Biology, University of California Berkeley, Berkeley, California, United States of America.

ABSTRACT
Sex chromosomes evolve distinctive types of chromatin from a pair of ancestral autosomes that are usually euchromatic. In Drosophila, the dosage-compensated X becomes enriched for hyperactive chromatin in males (mediated by H4K16ac), while the Y chromosome acquires silencing heterochromatin (enriched for H3K9me2/3). Drosophila autosomes are typically mostly euchromatic but the small dot chromosome has evolved a heterochromatin-like milieu (enriched for H3K9me2/3) that permits the normal expression of dot-linked genes, but which is different from typical pericentric heterochromatin. In Drosophila busckii, the dot chromosomes have fused to the ancestral sex chromosomes, creating a pair of 'neo-sex' chromosomes. Here we collect genomic, transcriptomic and epigenomic data from D. busckii, to investigate the evolutionary trajectory of sex chromosomes from a largely heterochromatic ancestor. We show that the neo-sex chromosomes formed <1 million years ago, but nearly 60% of neo-Y linked genes have already become non-functional. Expression levels are generally lower for the neo-Y alleles relative to their neo-X homologs, and the silencing heterochromatin mark H3K9me2, but not H3K9me3, is significantly enriched on silenced neo-Y genes. Despite rampant neo-Y degeneration, we find that the neo-X is deficient for the canonical histone modification mark of dosage compensation (H4K16ac), relative to autosomes or the compensated ancestral X chromosome, possibly reflecting constraints imposed on evolving hyperactive chromatin in an originally heterochromatic environment. Yet, neo-X genes are transcriptionally more active in males, relative to females, suggesting the evolution of incipient dosage compensation on the neo-X. Our data show that Y degeneration proceeds quickly after sex chromosomes become established through genomic and epigenetic changes, and are consistent with the idea that the evolution of sex-linked chromatin is influenced by its ancestral configuration.

No MeSH data available.


Related in: MedlinePlus

Karyotype and genome of D. busckii.A. Karyotype of D. busckii. The ancestral karyotype of Drosophila species consists of six chromosomal arms termed ‘Muller’s elements’. Muller-A element is the ancestral sex chromosome shared by all Drosophila species, and Muller-F is the dot chromosome. In D. busckii, the dot chromosome pair has fused to the ancestral X and Y chromosome and became the neo-X and neo-Y chromosome. B. Coverage and heterozygosity patterns of the D. busckii genome. For each chromosome of D. busckii (named after its homologous chromosome in D. melanogaster), we show mapped read coverage in male (blue) and female (red), and single nucleotide polymorphism (SNP) density (sites/kb) within 5kb non-overlapping windows along the chromosome. chrX shows a reduction of male coverage because the ancestral Y chromosome is completely degenerated in male D. busckii. The neo-sex (dot) chromosome shows similar coverage to autosomes, indicating that most neo-Y reads can still be mapped to the neo-X. The increase of male SNP density on the neo-sex chromosome indicates sequence divergence between the neo-X and neo-Y alleles.
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pgen.1005331.g001: Karyotype and genome of D. busckii.A. Karyotype of D. busckii. The ancestral karyotype of Drosophila species consists of six chromosomal arms termed ‘Muller’s elements’. Muller-A element is the ancestral sex chromosome shared by all Drosophila species, and Muller-F is the dot chromosome. In D. busckii, the dot chromosome pair has fused to the ancestral X and Y chromosome and became the neo-X and neo-Y chromosome. B. Coverage and heterozygosity patterns of the D. busckii genome. For each chromosome of D. busckii (named after its homologous chromosome in D. melanogaster), we show mapped read coverage in male (blue) and female (red), and single nucleotide polymorphism (SNP) density (sites/kb) within 5kb non-overlapping windows along the chromosome. chrX shows a reduction of male coverage because the ancestral Y chromosome is completely degenerated in male D. busckii. The neo-sex (dot) chromosome shows similar coverage to autosomes, indicating that most neo-Y reads can still be mapped to the neo-X. The increase of male SNP density on the neo-sex chromosome indicates sequence divergence between the neo-X and neo-Y alleles.

Mentions: Well-studied neo-sex chromosome systems are all derived from euchromatic autosomes, and studying a neo-sex chromosome that originated from an autosome with some features similar to heterochromatin may allow a more general understanding of the evolutionary principles of chromatin formation on sex chromosomes. Here, we collect data on the genome, transcriptome and epigenome of D. busckii, a species with a poorly characterized neo-sex chromosome derived by a fusion (and supposedly followed by a pericentric inversion on the X) between the ancestral sex chromosomes and the “heterochromatic” dot chromosome (Fig 1A) [17,18]. The age, and the extent of sequence, expression and epigenetic divergence of the neo-sex chromosomes of D. busckii are unknown, but the dot chromosome has an unusual evolutionary history and a unique chromatin structure. It was a sex chromosome in an ancestor of higher Diptera, and only reverted to an autosomal inheritance in the ancestor of the Drosophilidae family [19,20]. Studies on the assembled distal arm (~1.2Mb) of the D. melanogaster dot chromosome have revealed several features that distinguish it from other autosomes: it has a very low recombination rate and a high repeat content [21–23], harbors less than 100 genes [24] that have low codon usage bias[25] and which show evidence of reduced levels of positive and purifying selection [26]. Genes on the dot chromosome are embedded into a unique heterochromatin-like milieu that is regulated differently from canonical pericentric heterochromatin [21,27]. Both dot-linked genes and genes located in pericentric heterochromatin are enriched for the ‘silencing’ histone marks H3K9me2 and H3K9me3 and the heterochromatin protein HP1a relative to euchromatin, but show a depletion of these marks at the transcriptional start sites of active genes. In addition, expression of dot-linked genes (but not genes in pericentric heterochromatin) requires binding of the chromosomal protein Painting of Fourth (POF) and the histone methyltransferase EGG, and the gene bodies of transcribed genes show an enrichment of the histone modification H3K9me3 (but not H3K9me2) that is not observed at active genes located in pericentromeric heterochromatin. Genes on the dot chromosome that are not expressed and repetitive regions on the dot chromosome probably adopt a more general POF/EGG independent mechanism of heterochromatin packaging that is shared with pericentromeric regions [28].


Ancestral Chromatin Configuration Constrains Chromatin Evolution on Differentiating Sex Chromosomes in Drosophila.

Zhou Q, Bachtrog D - PLoS Genet. (2015)

Karyotype and genome of D. busckii.A. Karyotype of D. busckii. The ancestral karyotype of Drosophila species consists of six chromosomal arms termed ‘Muller’s elements’. Muller-A element is the ancestral sex chromosome shared by all Drosophila species, and Muller-F is the dot chromosome. In D. busckii, the dot chromosome pair has fused to the ancestral X and Y chromosome and became the neo-X and neo-Y chromosome. B. Coverage and heterozygosity patterns of the D. busckii genome. For each chromosome of D. busckii (named after its homologous chromosome in D. melanogaster), we show mapped read coverage in male (blue) and female (red), and single nucleotide polymorphism (SNP) density (sites/kb) within 5kb non-overlapping windows along the chromosome. chrX shows a reduction of male coverage because the ancestral Y chromosome is completely degenerated in male D. busckii. The neo-sex (dot) chromosome shows similar coverage to autosomes, indicating that most neo-Y reads can still be mapped to the neo-X. The increase of male SNP density on the neo-sex chromosome indicates sequence divergence between the neo-X and neo-Y alleles.
© Copyright Policy
Related In: Results  -  Collection

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Show All Figures
getmorefigures.php?uid=PMC4482674&req=5

pgen.1005331.g001: Karyotype and genome of D. busckii.A. Karyotype of D. busckii. The ancestral karyotype of Drosophila species consists of six chromosomal arms termed ‘Muller’s elements’. Muller-A element is the ancestral sex chromosome shared by all Drosophila species, and Muller-F is the dot chromosome. In D. busckii, the dot chromosome pair has fused to the ancestral X and Y chromosome and became the neo-X and neo-Y chromosome. B. Coverage and heterozygosity patterns of the D. busckii genome. For each chromosome of D. busckii (named after its homologous chromosome in D. melanogaster), we show mapped read coverage in male (blue) and female (red), and single nucleotide polymorphism (SNP) density (sites/kb) within 5kb non-overlapping windows along the chromosome. chrX shows a reduction of male coverage because the ancestral Y chromosome is completely degenerated in male D. busckii. The neo-sex (dot) chromosome shows similar coverage to autosomes, indicating that most neo-Y reads can still be mapped to the neo-X. The increase of male SNP density on the neo-sex chromosome indicates sequence divergence between the neo-X and neo-Y alleles.
Mentions: Well-studied neo-sex chromosome systems are all derived from euchromatic autosomes, and studying a neo-sex chromosome that originated from an autosome with some features similar to heterochromatin may allow a more general understanding of the evolutionary principles of chromatin formation on sex chromosomes. Here, we collect data on the genome, transcriptome and epigenome of D. busckii, a species with a poorly characterized neo-sex chromosome derived by a fusion (and supposedly followed by a pericentric inversion on the X) between the ancestral sex chromosomes and the “heterochromatic” dot chromosome (Fig 1A) [17,18]. The age, and the extent of sequence, expression and epigenetic divergence of the neo-sex chromosomes of D. busckii are unknown, but the dot chromosome has an unusual evolutionary history and a unique chromatin structure. It was a sex chromosome in an ancestor of higher Diptera, and only reverted to an autosomal inheritance in the ancestor of the Drosophilidae family [19,20]. Studies on the assembled distal arm (~1.2Mb) of the D. melanogaster dot chromosome have revealed several features that distinguish it from other autosomes: it has a very low recombination rate and a high repeat content [21–23], harbors less than 100 genes [24] that have low codon usage bias[25] and which show evidence of reduced levels of positive and purifying selection [26]. Genes on the dot chromosome are embedded into a unique heterochromatin-like milieu that is regulated differently from canonical pericentric heterochromatin [21,27]. Both dot-linked genes and genes located in pericentric heterochromatin are enriched for the ‘silencing’ histone marks H3K9me2 and H3K9me3 and the heterochromatin protein HP1a relative to euchromatin, but show a depletion of these marks at the transcriptional start sites of active genes. In addition, expression of dot-linked genes (but not genes in pericentric heterochromatin) requires binding of the chromosomal protein Painting of Fourth (POF) and the histone methyltransferase EGG, and the gene bodies of transcribed genes show an enrichment of the histone modification H3K9me3 (but not H3K9me2) that is not observed at active genes located in pericentromeric heterochromatin. Genes on the dot chromosome that are not expressed and repetitive regions on the dot chromosome probably adopt a more general POF/EGG independent mechanism of heterochromatin packaging that is shared with pericentromeric regions [28].

Bottom Line: We show that the neo-sex chromosomes formed <1 million years ago, but nearly 60% of neo-Y linked genes have already become non-functional.Expression levels are generally lower for the neo-Y alleles relative to their neo-X homologs, and the silencing heterochromatin mark H3K9me2, but not H3K9me3, is significantly enriched on silenced neo-Y genes.Yet, neo-X genes are transcriptionally more active in males, relative to females, suggesting the evolution of incipient dosage compensation on the neo-X.

View Article: PubMed Central - PubMed

Affiliation: Department of Integrative Biology, University of California Berkeley, Berkeley, California, United States of America.

ABSTRACT
Sex chromosomes evolve distinctive types of chromatin from a pair of ancestral autosomes that are usually euchromatic. In Drosophila, the dosage-compensated X becomes enriched for hyperactive chromatin in males (mediated by H4K16ac), while the Y chromosome acquires silencing heterochromatin (enriched for H3K9me2/3). Drosophila autosomes are typically mostly euchromatic but the small dot chromosome has evolved a heterochromatin-like milieu (enriched for H3K9me2/3) that permits the normal expression of dot-linked genes, but which is different from typical pericentric heterochromatin. In Drosophila busckii, the dot chromosomes have fused to the ancestral sex chromosomes, creating a pair of 'neo-sex' chromosomes. Here we collect genomic, transcriptomic and epigenomic data from D. busckii, to investigate the evolutionary trajectory of sex chromosomes from a largely heterochromatic ancestor. We show that the neo-sex chromosomes formed <1 million years ago, but nearly 60% of neo-Y linked genes have already become non-functional. Expression levels are generally lower for the neo-Y alleles relative to their neo-X homologs, and the silencing heterochromatin mark H3K9me2, but not H3K9me3, is significantly enriched on silenced neo-Y genes. Despite rampant neo-Y degeneration, we find that the neo-X is deficient for the canonical histone modification mark of dosage compensation (H4K16ac), relative to autosomes or the compensated ancestral X chromosome, possibly reflecting constraints imposed on evolving hyperactive chromatin in an originally heterochromatic environment. Yet, neo-X genes are transcriptionally more active in males, relative to females, suggesting the evolution of incipient dosage compensation on the neo-X. Our data show that Y degeneration proceeds quickly after sex chromosomes become established through genomic and epigenetic changes, and are consistent with the idea that the evolution of sex-linked chromatin is influenced by its ancestral configuration.

No MeSH data available.


Related in: MedlinePlus