Abstract
The term heterochromatin has been long considered synonymous with gene silencing, but it is now clear that the presence of transcribed genes embedded in pericentromeric heterochromatin is a conserved feature in the evolution of eukaryotic genomes. Several studies have addressed the epigenetic changes that enable the expression of genes in pericentric heterochromatin, yet little is known about the evolutionary processes through which this has occurred. By combining genome annotation analysis and high-resolution cytology, we have identified and mapped 53 orthologs of D. melanogaster heterochromatic genes in the genomes of two evolutionarily distant species, D. pseudoobscura and D. virilis. Our results show that the orthologs of the D. melanogaster heterochromatic genes are clustered at three main genomic regions in D. virilis and D. pseudoobscura. In D. virilis, the clusters lie in the middle of euchromatin, while those in D. pseudoobscura are located in the proximal portion of the chromosome arms. Some orthologs map to the corresponding Muller C element in D. pseudoobscura and D. virilis, while others localize on the Muller B element, suggesting that chromosomal rearrangements that have been instrumental in the fusion of two separate elements involved the progenitors of genes currently located in D. melanogaster heterochromatin. These results demonstrate an evolutionary repositioning of gene clusters from ancestral locations in euchromatin to the pericentromeric heterochromatin of descendent D. melanogaster chromosomes. Remarkably, in both D. virilis and D. pseudoobscura the gene clusters show a conserved association with the HP1a protein, one of the most highly evolutionarily conserved epigenetic marks. In light of these results, we suggest a new scenario whereby ancestral HP1-like proteins (and possibly other epigenetic marks) may have contributed to the evolutionary repositioning of gene clusters into heterochromatin.
Highlights
The organization of eukaryotic genomes into euchromatin and heterochromatin represents one of the most important and still unsolved aspects of genome evolution
By combining genome annotation analysis and high-resolution cytology, we have performed a comparative mapping of the orthologs of 53 single-copy genes of D. melanogaster heterochromatin, in the genomes of D. pseudoobscura and D. virilis evolutionarily distant species
The results of our work are consistent with a scenario where the D. melanogaster heterochromatin genes arose through an evolutionary repositioning from a euchromatic location (D. virilis) to heterochromatin, passing through an intermediate location in regions associated with distal heterochromatin (D. pseudoobscura)
Summary
The organization of eukaryotic genomes into euchromatin and heterochromatin represents one of the most important and still unsolved aspects of genome evolution. A signature feature of heterochromatin is its ability to silence euchromatic genes that are brought within a heterochromatic environment following a chromosome rearrangement or a transposition event, a well-known phenomenon called position effect variegation (PEV) which provides an important model for studying the mechanisms regulating gene repression by chromatin modifications [20,21,22,23,24].Yet, the single-copy genes embedded in the heterochromatin of D. melanogaster are bound by specific proteins [25,26,27], show a pattern of modified histones [18] and their proper expression depends on their heterochromatic location [28,29], despite the fact that they are transcribed from promoter regions sharing basic similarities with those of euchromatic genes [30,31]
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