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LTR retroelements are intrinsic components of transcriptional networks in frogs.
Grau JH
,
Poustka AJ
,
Meixner M
,
Plötner J
.
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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.
Figure 1.
Classification and structure of LTR retroelements in the frog genome and transcriptomes. Maximum-likelihood (ML) trees calculated on the basis of 256 known RT domains of eukaryotic LTR REs including amino acid sequences obtained from the Silurana tropicalis genome (a) and the transcriptomes of Pelophylax lessonae
(b). Diagrammatic presentation of LTR REs (c) found in the Silurana genome (blue) and in the transcriptome of P. lessonae (red). The thin lines represent the overall length of the retroelement including the LTRs, while thick bars depict open reading frames for aspartic proteinase (AP), chromo domain (CHR), envelope protein (ENV), group-specific antigen (GAG), integrase (INT), RNase (RN), and reverse transcriptase (RT). Frameshifts are indicated by asterisks (*).
Figure 2.
Diversity and expression patterns of LTR retroelements in the frog genome and transcriptomes. (a) Diversity of LTR REs in the genome of Silurana and in the frogs transcriptomes analyzed. (b) Number of LTR RE copies in the Silurana genome; (c) Proliferation patterns based on average relatedness of LTR REs in the Silurana genome. The average relatedness was calculated on the basis of amino acids as LOG (â (Alignment coverage *Alignment score)), in which a higher relatedness score indicates that the elements within that group are closer related to one another. (d) Arithmetic means of relative NRC values calculated for brain (B), heart (H), liver (L), and muscle (M) of S. tropicalis (left points) and P. lessonae (right points). (e) Relative amount of LTR REs in different frog transcriptomes.
Figure 3.
Normalized read counts and relative amount of expression of LTR retroelement (LTR RE) transcripts throughout the developmental progression of
S. tropicalis
progession. The presence of each type of LTR RE found within the transcriptome of S. tropicalis throughout 23 distinct developmental stages is summarized.
Figure 4.
Work flow diagram summarizing data flow from sequencing to statistical analysis. Abbreviations used in the Figure: DB, database; LTR REs, long terminal repeat retroelements.
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