Chromosome Research

, Volume 23, Issue 3, pp 597–613 | Cite as

Helitrons shaping the genomic architecture of Drosophila: enrichment of DINE-TR1 in α- and β-heterochromatin, satellite DNA emergence, and piRNA expression

  • Guilherme B. Dias
  • Pedro Heringer
  • Marta Svartman
  • Gustavo C. S. Kuhn
Original Article


Drosophila INterspersed Elements (DINEs) constitute an abundant but poorly understood group of Helitrons present in several Drosophila species. The general structure of DINEs includes two conserved blocks that may or not contain a region with tandem repeats in between. These central tandem repeats (CTRs) are similar within species but highly divergent between species. It has been assumed that CTRs have independent origins. Herein, we identify a subset of DINEs, termed DINE-TR1, which contain homologous CTRs of approximately 150 bp. We found DINE-TR1 in the sequenced genomes of several Drosophila species and in Bactrocera tryoni (Acalyptratae, Diptera). However, interspecific high sequence identity (∼88 %) is limited to the first ∼30 bp of each tandem repeat, implying that evolutionary constraints operate differently over the monomer length. DINE-TR1 is unevenly distributed across the Drosophila phylogeny. Nevertheless, sequence analysis suggests vertical transmission. We found that CTRs within DINE-TR1 have independently expanded into satellite DNA-like arrays at least twice within Drosophila. By analyzing the genome of Drosophila virilis and Drosophila americana, we show that DINE-TR1 is highly abundant in pericentromeric heterochromatin boundaries, some telomeric regions and in the Y chromosome. It is also present in the centromeric region of one autosome from D. virilis and dispersed throughout several euchromatic sites in both species. We further found that DINE-TR1 is abundant at piRNA clusters, and small DINE-TR1-derived RNA transcripts (25 nt) are predominantly expressed in the testes and the ovaries, suggesting active targeting by the piRNA machinery. These features suggest potential piRNA-mediated regulatory roles for DINEs at local and genome-wide scales in Drosophila.


Drosophila virilis Drosophila americana Transposable element Genome evolution Helitrons 



Akaike Information Criterion


Central tandem repeats


Drosophila INterspersed Elements


Fluorescence in situ hybridization


Inverted repeat




Male-specific lethal complex


Piwi-interacting RNA


Satellite DNA


Small interfering RNA


Subtree pruning and regrafting algorithm


Subterminal inverted repeats


Transposable element


Tandem repeat



We are grateful for the anonymous reviewers’ comments on the manuscript. This work was supported by grants from “Fundação de Amparo à Pesquisa do Estado de Minas Gerais” (FAPEMIG) (Proc: APQ-01563-14), “Programa Institucional de Auxílio à Pesquisa de Doutores Recém-Contratados da Universidade Federal de Minas Gerais,” “Conselho Nacional de Desenvolvimento Científico e Tecnológico” (CNPq), and a doctoral fellowship from “Coordenação de Aperfeiçoamento de Pessoal de Nível Superior” (CAPES) to GD.

Supplementary material

10577_2015_9480_MOESM1_ESM.pdf (150 kb)
ESM 1 (PDF 149 kb)


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Authors and Affiliations

  • Guilherme B. Dias
    • 1
  • Pedro Heringer
    • 1
  • Marta Svartman
    • 1
  • Gustavo C. S. Kuhn
    • 1
  1. 1.Departamento de Biologia GeralUniversidade Federal de Minas GeraisBelo HorizonteBrazil

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