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Open Access Research article

LTR retroelements are intrinsic components of transcriptional networks in frogs

José Horacio Grau12*, Albert J Poustka13, Martin Meixner4 and Jörg Plötner2

Author Affiliations

1 Dahlem Center for Genome Research and Medical Systems Biology, Fabeckstraße 60-62, 14195 Berlin, Germany

2 Museum für Naturkunde Berlin, Leibniz-Institut für Evolutions- und Biodiversitätsforschung, Invalidenstraße 43, 10115 Berlin, Germany

3 Max-Planck-Institut für Molekulare Genetik, AG Evolution and Development, Ihnestraße 73-75, 14195 Berlin, Germany

4 Services in Molecular Biology GmbH, Rudolf-Breitscheid-Str. 70, 15562 Rüdersdorf, Germany

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BMC Genomics 2014, 15:626  doi:10.1186/1471-2164-15-626

Published: 23 July 2014

Abstract

Background

LTR retroelements (LTR REs) constitute a major group of transposable elements widely distributed in eukaryotic genomes. Through their own mechanism of retrotranscription LTR REs enrich the genomic landscape by providing genetic variability, thus contributing to genome structure and organization. Nonetheless, transcriptomic activity of LTR REs still remains an obscure domain within cell, developmental, and organism biology.

Results

Here we present a first comparative analysis of LTR REs for anuran amphibians based on a full depth coverage transcriptome of the European pool frog, Pelophylax lessonae, the genome of the African clawed frog, Silurana tropicalis (release v7.1), and additional transcriptomes of S. tropicalis and Cyclorana alboguttata. We identified over 1000 copies of LTR REs from all four families (Bel/Pao, Ty1/Copia, Ty3/Gypsy, Retroviridae) in the genome of S. tropicalis and discovered transcripts of several of these elements in all RNA-seq datasets analyzed. Elements of the Ty3/Gypsy family were most active, especially Amn-san elements, which accounted for approximately 0.27% of the genome in Silurana. Some elements exhibited tissue specific expression patterns, for example Hydra1.1 and MuERV-like elements in Pelophylax. In S. tropicalis considerable transcription of LTR REs was observed during embryogenesis as soon as the embryonic genome became activated, i.e. at midblastula transition. In the course of embryonic development the spectrum of transcribed LTR REs changed; during gastrulation and neurulation MuERV-like and SnRV like retroviruses were abundantly transcribed while during organogenesis transcripts of the XEN1 retroviruses became much more active.

Conclusions

The differential expression of LTR REs during embryogenesis in concert with their tissue-specificity and the protein domains they encode are evidence for the functional roles these elements play as integrative parts of complex regulatory networks. Our results support the meanwhile widely accepted concept that retroelements are not simple “junk DNA” or “harmful genomic parasites” but essential components of the transcriptomic machinery in vertebrates.

Keywords:
LTR retroelements; Silurana; Pelophylax; Anura; RNAseq; Transcriptome; Embryogenesis