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Analysis of plant LTR-retrotransposons at the fine-scale family level reveals individual molecular patterns.

ABSTRACT: BACKGROUND: Sugarcane is an important crop worldwide for sugar production and increasingly, as a renewable energy source. Modern cultivars have polyploid, large complex genomes, with highly unequal contributions from ancestral genomes. Long Terminal Repeat retrotransposons (LTR-RTs) are the single largest components of most plant genomes and can substantially impact the genome in many ways. It is therefore crucial to understand their contribution to the genome and transcriptome, however a detailed study of LTR-RTs in sugarcane has not been previously carried out. RESULTS: Sixty complete LTR-RT elements were classified into 35 families within four Copia and three Gypsy lineages. Structurally, within lineages elements were similar, between lineages there were large size differences. FISH analysis resulted in the expected pattern of Gypsy/heterochromatin, Copia/euchromatin, but in two lineages there was localized clustering on some chromosomes. Analysis of related ESTs and RT-PCR showed transcriptional variation between tissues and families. Four distinct patterns were observed in sRNA mapping, the most unusual of which was that of Ale1, with very large numbers of 24nt sRNAs in the coding region. The results presented support the conclusion that distinct small RNA-regulated pathways in sugarcane target the lineages of LTR-RT elements. CONCLUSIONS: Individual LTR-RT sugarcane families have distinct structures, and transcriptional and regulatory signatures. Our results indicate that in sugarcane individual LTR-RT families have distinct behaviors and can potentially impact the genome in diverse ways. For instance, these transposable elements may affect nearby genes by generating a diverse set of small RNA's that trigger gene silencing mechanisms. There is also some evidence that ancestral genomes contribute significantly different element numbers from particular LTR-RT lineages to the modern sugarcane cultivar genome.

SUBMITTER: Domingues DS

PROVIDER: S-EPMC3352295 | biostudies-literature | 2012

REPOSITORIES: biostudies-literature

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Analysis of plant LTR-retrotransposons at the fine-scale family level reveals individual molecular patterns.

Domingues Douglas S DS Cruz Guilherme M Q GM Metcalfe Cushla J CJ Nogueira Fabio T S FT Vicentini Renato R Alves Cristiane de S Cde S Van Sluys Marie-Anne MA

BMC genomics 20120416

<h4>Background</h4>Sugarcane is an important crop worldwide for sugar production and increasingly, as a renewable energy source. Modern cultivars have polyploid, large complex genomes, with highly unequal contributions from ancestral genomes. Long Terminal Repeat retrotransposons (LTR-RTs) are the single largest components of most plant genomes and can substantially impact the genome in many ways. It is therefore crucial to understand their contribution to the genome and transcriptome, however a ...[more]

PMID: 22507400

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Project description:BACKGROUND: Retrotransposons are transposable elements that proliferate within eukaryotic genomes through a process involving reverse transcription. The numbers of retrotransposons within genomes and differences between closely related species may yield insight into the evolutionary history of the elements. Less is known about the ongoing dynamics of retrotransposons, as analysis of genome sequences will only reveal insertions of retrotransposons that are fixed--or near fixation--in the population or strain from which genetic material has been extracted for sequencing. One pre-requisite for retrotransposition is transcription of the elements. Given their intrinsic sequence redundancy, transcriptome-level analyses of transposable elements are scarce. We have used recently published transcriptome data from the fission yeast Schizosaccharomyces pombe to assess the ability to detect and describe transcriptional activity from Long Terminal Repeat (LTR) retrotransposons. LTR retrotransposons are normally flanked by two LTR sequences. However, the majority of LTR sequences in S. pombe exist as solitary LTRs, i.e. as single terminal repeat sequences not flanking a retrotransposon. Transcriptional activity was analysed for both full-length LTR retrotransposons and solitary LTRs. RESULTS: Two independent sets of transcriptome data reveal the presence of full-length, polyadenylated transcripts from LTR retrotransposons in S. pombe during growth phase in rich medium. The redundancy of retrotransposon sequences makes it difficult to assess which elements are transcriptionally active, but data strongly indicates that only a subset of the LTR retrotransposons contribute significantly to the detected transcription. A considerable level of reverse strand transcription is also detected. Equal levels of transcriptional activity are observed from both strands of solitary LTR sequences. Transcriptome data collected during meiosis suggests that transcription of solitary LTRs is correlated with the transcription of nearby protein-coding genes. CONCLUSIONS: Presumably, the host organism negatively regulates proliferation of LTR retrotransposons. The finding of considerable transcriptional activity of retrotransposons suggests that part of this regulation is likely to take place at a post-transcriptional level. Alternatively, the transcriptional activity may signify a hitherto unrecognized activity level of retrotransposon proliferation. Our findings underline the usefulness of transcriptome data in elucidating dynamics in retrotransposon transcription.

Project description:Sireviruses are an ancient and plant-specific LTR retrotransposon genus. They possess a unique genome structure that is characterized by a plethora of highly conserved sequence motifs in key domains of the non-coding genome, and often, by the presence of an envelope-like gene. Recently, their crucial role in the organization of the maize genome, where Sireviruses occupy approximately 21% of its nuclear content, was revealed, followed by an analysis of their distribution across the plant kingdom. It is now suggested that Sireviruses have been a major mediator of the evolution of many plant genomes. However, the name 'Sirevirus' has caused confusion in the scientific community in regards to their classification within the LTR retrotransposon order and their relationship with viruses - a situation that is not unique to Sireviruses, but also affects other LTR retrotransposon genera. Here, we clarify the phylogenetic position of Sireviruses as typical LTR retrotransposons of the Copia superfamily and explain that the confusion stems from the discrepancy in the categorization of LTR retrotransposons by the two main classification systems: the International Committee on the Taxonomy of Viruses (ICTV) system and the unified classification system for eukaryotic transposable elements. While the name 'Sirevirus' has been given by ICTV, we show that the transposable element system, which is more suitable for eukaryotic genome studies, lacks an appropriate taxonomic level for describing them. We urge for this inconsistency to be addressed. Finally, we provide data suggesting that of the three ICTV-proposed genera of the Pseudoviridae (that is, Copia) family, only Sireviruses form a monophyletic group, while the phylogenetic distinction between Pseudoviruses and Hemiviruses is unclear. We conclude that because of their ongoing important contribution to the classification of transposable elements, these schemes need to be frequently revisited and revised - as shown by the example of the Sirevirus LTR retrotransposon genus.

Project description:BackgroundThe three superfamilies of Long Terminal Repeat (LTR) retrotransposons are a widespread kind of transposable element and a major factor in eukaryotic genome evolution. In metazoans, recent studies suggested that Copia LTR-retrotransposons display specific dynamic compared to the more abundant and diverse Gypsy elements. Indeed, Copia elements show a relative scarcity and the prevalence of only a few clades in specific hosts. Thus, BEL/Pao seems to be the second most abundant superfamily. However, the generality of these assumptions remains to be assessed. Therefore, we carried out the first large-scale comparative genomic analysis of LTR-retrotransposons in molluscs. The aim of this study was to analyse the diversity, copy numbers, genomic proportions and distribution of LTR-retrotransposons in a large host phylum.ResultsWe compare nine genomes of molluscs and further added LTR-retrotransposons sequences detected in databases for 47 additional species. We identified 1709 families, which enabled us to define 31 clades. We show that clade richness was highly dependent on the considered superfamily. We found only three Copia clades, including GalEa and Hydra which appear to be widely distributed and highly dominant as they account for 96% of the characterised Copia elements. Among the seven BEL/Pao clades identified, Sparrow and Surcouf are characterised for the first time. We find no BEL or Pao elements, but the rare clades Dan and Flow are present in molluscs. Finally, we characterised 21 Gypsy clades, only five of which had been previously described, the C-clade being the most abundant one. Even if they are found in the same number of host species, Copia elements are clearly less abundant than BEL/Pao elements in copy number or genomic proportions, while Gypsy elements are always the most abundant ones whatever the parameter considered.ConclusionsOur analysis confirms the contrasting dynamics of Copia and Gypsy elements in metazoans and indicates that BEL/Pao represents the second most abundant superfamily, probably reflecting an intermediate dynamic. Altogether, the data obtained in several taxa highly suggest that these patterns can be generalised for most metazoans. Finally, we highlight the importance of using database information in complement of genome analyses when analyzing transposable element diversity.

Dataset Information

Analysis of plant LTR-retrotransposons at the fine-scale family level reveals individual molecular patterns.

Publications

Analysis of plant LTR-retrotransposons at the fine-scale family level reveals individual molecular patterns.

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