Expression of Transposable Elements in Neural Tissues during Xenopus Development

Fernando Faunes,John S Mattick,Natalia Sanchez,Leonardo Almonacid,Alex W Slater,Ryan J Taft,Francisco Melo,Dasfne Lee-Liu,Juan Larrain,Tomas Norambuena,Gonzalo H Olivares,Mauricio Moreno,Gert Jan C Veenstra

doi:10.1371/journal.pone.0022569

Abstract

Transposable elements comprise a large proportion of animal genomes. Transposons can have detrimental effects on genome stability but also offer positive roles for genome evolution and gene expression regulation. Proper balance of the positive and deleterious effects of transposons is crucial for cell homeostasis and requires a mechanism that tightly regulates their expression. Herein we describe the expression of DNA transposons of the Tc1/mariner superfamily during Xenopus development. Sense and antisense transcripts containing complete Tc1-2_Xt were detected in Xenopus embryos. Both transcripts were found in zygotic stages and were mainly localized in Spemann's organizer and neural tissues. In addition, the Tc1-like elements Eagle, Froggy, Jumpy, Maya, Xeminos and TXr were also expressed in zygotic stages but not oocytes in X. tropicalis. Interestingly, although Tc1-2_Xt transcripts were not detected in Xenopus laevis embryos, transcripts from other two Tc1-like elements (TXr and TXz) presented a similar temporal and spatial pattern during X. laevis development. Deep sequencing analysis of Xenopus tropicalis gastrulae showed that PIWI-interacting RNAs (piRNAs) are specifically derived from several Tc1-like elements. The localized expression of Tc1-like elements in neural tissues suggests that they could play a role during the development of the Xenopus nervous system.

Highlights

The complexity of genomes and their transcriptomes has been recognized [1]
It is important to mention that Repbase contains an element identified as Tc1-2_Xt but it corresponds to a different element, identified as Tc1DR3 in RepeatMasker and as maya according to Sinzelle et al [22]
The Tc1-2_Xt family has an average length of 1,581 bp and contains the typical structure of DNA transposon organization; the transposase ORF is flanked by two 199 bp Inverted Repeats (IRs) which include two 17 bp direct repeats (DRs) (Figure 1A)

Summary

Introduction

The complexity of genomes and their transcriptomes has been recognized [1]. Transposable elements comprise a large proportion of animal genomes, for example 20% in D. melanogaster, 36% in X. tropicalis and 45% in humans [3,4]. They are classified into two classes according to their mode of transposition [5]. Class I elements correspond to retrotransposons, which transpose through an RNA intermediate. Class II elements are DNA transposons and transpose through a ‘‘cut and paste’’ mechanism. Retrotransposons comprise 80% of elements in D. melanogaster and 90% in humans [6]. 72% of all transposable elements are DNA transposons in X. tropicalis [3]

Methods

Results

Conclusion