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

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Abstract

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.

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Abbreviations

AIC:

Akaike Information Criterion

CTRs:

Central tandem repeats

DINEs:

Drosophila INterspersed Elements

FISH:

Fluorescence in situ hybridization

IR:

Inverted repeat

miRNA:

microRNA

MSL:

Male-specific lethal complex

piRNA:

Piwi-interacting RNA

satDNA:

Satellite DNA

siRNA:

Small interfering RNA

SPR:

Subtree pruning and regrafting algorithm

subTIRs:

Subterminal inverted repeats

TE:

Transposable element

TR:

Tandem repeat

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Acknowledgments

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.

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  1. Departamento de Biologia Geral, Universidade Federal de Minas Gerais, Belo Horizonte, MG, Brazil

    Guilherme B. Dias, Pedro Heringer, Marta Svartman & Gustavo C. S. Kuhn

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  1. Guilherme B. Dias
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  2. Pedro Heringer
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  3. Marta Svartman
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  4. Gustavo C. S. Kuhn
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Correspondence to Gustavo C. S. Kuhn.

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Dias, G.B., Heringer, P., Svartman, M. et al. Helitrons shaping the genomic architecture of Drosophila: enrichment of DINE-TR1 in α- and β-heterochromatin, satellite DNA emergence, and piRNA expression. Chromosome Res 23, 597–613 (2015). https://doi.org/10.1007/s10577-015-9480-x

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