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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

Phylogeny of D. busckii.We used 6189 orthologous gene pairs from 9 Diptera species and constructed a phylogenomic tree. Although the bootstrap value at the ancestral node of D. busckii and D. albomicans is low, D. busckii is grouped with high confidence within the Drosophila subgroup instead of as a sister group to all Drosophila species, as previously hypothesized [16,30].
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pgen.1005331.g002: Phylogeny of D. busckii.We used 6189 orthologous gene pairs from 9 Diptera species and constructed a phylogenomic tree. Although the bootstrap value at the ancestral node of D. busckii and D. albomicans is low, D. busckii is grouped with high confidence within the Drosophila subgroup instead of as a sister group to all Drosophila species, as previously hypothesized [16,30].

Mentions: The phylogenetic relationship of D. busckii within the Drosophila genus is unclear. Some studies placed it as a sister to all other Drosophila species [16,30], while others put it within the Drosophila subgenus [35]. This uncertainty in the phylogenetic position of D. busckii could have resulted from the small number of genes that were previously investigated, and we use whole-genome sequence alignments of representative Drosophila species and other Drosophilidae, to generate a phylogenomic tree. Our alignments include D. melanogaster, D. pseudoobscura and D. willistoni from the Sophophora subgenus; D. albomicans [11], D. grimshawi and D. virilis from the Drosophila subgenus, D. busckii and two recently sequenced Diptera species within the Drosophilidae family: Scaptodrosophila lebanonensis [36] and Phortica variegata [19] as outgroups to the Drosophila genus [35–37]. In total, we aligned CDS sequences of 6189 orthologous genes spanning a total of 19.1Mb from each species and acquired a consensus tree with high bootstrapping values (Fig 2). D. busckii consistently clusters with the Drosophila subgenus species (D. albomicans, D. grimshawi and D. virilis) rather than being placed at the base of all Drosophila. This phylogenetic analysis suggests that D. busckii is not a member of an early divergent Drosophila lineage, but originated within the Drosophila subgenus.


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

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

Phylogeny of D. busckii.We used 6189 orthologous gene pairs from 9 Diptera species and constructed a phylogenomic tree. Although the bootstrap value at the ancestral node of D. busckii and D. albomicans is low, D. busckii is grouped with high confidence within the Drosophila subgroup instead of as a sister group to all Drosophila species, as previously hypothesized [16,30].
© Copyright Policy
Related In: Results  -  Collection

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

pgen.1005331.g002: Phylogeny of D. busckii.We used 6189 orthologous gene pairs from 9 Diptera species and constructed a phylogenomic tree. Although the bootstrap value at the ancestral node of D. busckii and D. albomicans is low, D. busckii is grouped with high confidence within the Drosophila subgroup instead of as a sister group to all Drosophila species, as previously hypothesized [16,30].
Mentions: The phylogenetic relationship of D. busckii within the Drosophila genus is unclear. Some studies placed it as a sister to all other Drosophila species [16,30], while others put it within the Drosophila subgenus [35]. This uncertainty in the phylogenetic position of D. busckii could have resulted from the small number of genes that were previously investigated, and we use whole-genome sequence alignments of representative Drosophila species and other Drosophilidae, to generate a phylogenomic tree. Our alignments include D. melanogaster, D. pseudoobscura and D. willistoni from the Sophophora subgenus; D. albomicans [11], D. grimshawi and D. virilis from the Drosophila subgenus, D. busckii and two recently sequenced Diptera species within the Drosophilidae family: Scaptodrosophila lebanonensis [36] and Phortica variegata [19] as outgroups to the Drosophila genus [35–37]. In total, we aligned CDS sequences of 6189 orthologous genes spanning a total of 19.1Mb from each species and acquired a consensus tree with high bootstrapping values (Fig 2). D. busckii consistently clusters with the Drosophila subgenus species (D. albomicans, D. grimshawi and D. virilis) rather than being placed at the base of all Drosophila. This phylogenetic analysis suggests that D. busckii is not a member of an early divergent Drosophila lineage, but originated within the Drosophila subgenus.

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