LTR retroelements are intrinsic components of transcriptional networks in frogs

Abstract

BackgroundLTR 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.ResultsHere 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.ConclusionsThe 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.Electronic supplementary materialThe online version of this article (doi:10.1186/1471-2164-15-626) contains supplementary material, which is available to authorized users.

Heterochromatic histone modifications at transposons in Xenopus tropicalis embryos

“…It has been shown in human, mouse and frogs that TEs are actively and dynamically transcribed during early embryogenesis (Grau et al 2014; Levin & Moran 2011). TEs contain functional elements, such as enhancers, promoters, polyadenylation signals, insulators and transcription factor binding sites.…”

A novel class III endogenous retrovirus with a class I envelope gene in African frogs with an intact genome and developmentally regulated transcripts in Xenopus tropicalis

“…Embryonic expression of XtERV-S in mid-stage embryos differs from that of mouse ERV-L which peaks at the 2 cell stage and decreases at the 8 cell stage [ 65 , 68 ]. A previous genome wide analysis that examined expression of X. tropicalis LTR retroelements similarly found that expression of this set of retroelements is activated at mid-blastula [ 69 ]. These data taken together show that XtERV-S is likely transcribed, that transcription is particularly active during specific stages of development, and that tagged transfected gag can produce protein that shows the expected cellular distribution.…”

“…The chart shows the total number of reads per kilobase per million (RPKM) mapped to the provirus and the reads mapping to LTR, gag, pol, and env. The developmental stages and events are indicated, including MBT (mid-blastula transition); the red arrow represents the transcriptional transition from maternal mRNA to zygote genome transcribed mRNAs; the green arrow represents the beginning of the tadpole stage wide analysis that examined expression of X. tropicalis LTR retroelements similarly found that expression of this set of retroelements is activated at mid-blastula [69]. These data taken together show that XtERV-S is likely transcribed, that transcription is particularly active during specific stages of development, and that tagged transfected gag can produce protein that shows the expected cellular distribution.…”

Endogenous Retroviruses Augment Amphibian (Xenopus laevis) Tadpole Antiviral Protection

“…While to our knowledge Xen1 is the only ERV described within the X. laevis genome, a number of ERVs have been described in other amphibian species, including the related X. tropicalis (58). It will be interesting to learn with further studies which of these have been conserved across amphibian evolution and how these respective ERVs contribute to amphibian immunity and physiology.…”