On the evolution of Yeti, a Drosophila melanogaster heterochromatin gene

PLoS One. 2014 Nov 18;9(11):e113010. doi: 10.1371/journal.pone.0113010. eCollection 2014.

Abstract

Constitutive heterochromatin is a ubiquitous and still unveiled component of eukaryotic genomes, within which it comprises large portions. Although constitutive heterochromatin is generally considered to be transcriptionally silent, it contains a significant variety of sequences that are expressed, among which about 300 single-copy coding genes have been identified by genetic and genomic analyses in the last decades. Here, we report the results of the evolutionary analysis of Yeti, an essential gene of Drosophila melanogaster located in the deep pericentromeric region of chromosome 2R. By FISH, we showed that Yeti maintains a heterochromatin location in both D. simulans and D. sechellia species, closely related to D. melanogaster, while in the more distant species e.g., D. pseudoobscura and D. virilis, it is found within euchromatin, in the syntenic chromosome Muller C, that corresponds to the 2R arm of D. melanogaster chromosome 2. Thus, over evolutionary time, Yeti has been resident on the same chromosomal element, but it progressively moved closer to the pericentric regions. Moreover, in silico reconstruction of the Yeti gene structure in 19 Drosophila species and in 5 non-drosophilid dipterans shows a rather stable organization during evolution. Accordingly, by PCR analysis and sequencing, we found that the single intron of Yeti does not undergo major intraspecies or interspecies size changes, unlike the introns of other essential Drosophila heterochromatin genes, such as light and Dbp80. This implicates diverse evolutionary forces in shaping the structural organization of genes found within heterochromatin. Finally, the results of dS - dN tests show that Yeti is under negative selection both in heterochromatin and euchromatin, and indicate that the change in genomic location did not affected significantly the molecular evolution of the gene. Together, the results of this work contribute to our understanding of the evolutionary dynamics of constitutive heterochromatin in the genomes of higher eukaryotes.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Base Sequence
  • Carrier Proteins / genetics*
  • Chromosome Mapping
  • Drosophila Proteins / genetics*
  • Drosophila melanogaster / genetics*
  • Evolution, Molecular*
  • Gene Components
  • Heterochromatin / genetics*
  • In Situ Hybridization, Fluorescence
  • Molecular Sequence Data
  • Polymerase Chain Reaction
  • Sequence Analysis, DNA
  • Species Specificity

Substances

  • Carrier Proteins
  • Drosophila Proteins
  • Heterochromatin
  • Yeti protein, Drosophila

Grants and funding

This research was supported by grants from Ministero dell'Università e della Ricerca- Miur (Prin 2008), Istituto Pasteur-Fondazione Cenci-Bolognetti and Fondazione Roma terzo settore. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.