Evolutionary dynamics of transposable elements in prokaryotes and eukaryotes

This paper summarizes some recent theories about the evolution of transposable genetic elements in outbreeding, sexual eukaryotic organisms. The evolutionary possibilities available to self-replicating transposable elements are shown to vary depending on the reproductive biology of the host genome. This effect can be used to explain, in part, the differences in abundance of transposable elements between prokaryotes and eukaryotes. It is argued that the pattern of sexual outbreeding seen in mammals and plants is especially favorable to the spread of transposons. Moreover, because transposon spread is facilitated by zygote formation, the evolutionary origin of sexual conjugation may have been due to selection on transposon-encoded genes. Finally, evidence is also presented that introns could have originated as transposable genetic elements.     

Evolutionary dynamics of transposable elements during silkworm domestication

Although there are some documented examples on population dynamics of transposable elements (TEs) in model organisms, the evolutionary dynamics of TEs in domesticated species has not been systematically investigated. The objective of this study is to understand population dynamics of TEs during silkworm domestication. In this work, using transposon-display we examined the polymorphism of seven TE families [they represent about 59% of silkworm (Bombyx mori) total TE content] in four domesticated silkworm populations and one wild silkworm population. Maximum likelihood (ML) was used to estimate selection pressure. Population differentiation and structure were performed by using AMOVA analysis and program DISTRUCT, respectively. The results of transposon-display showed that significant differentiation occurred between the domesticated silkworm and wild silkworm. These TEs have experienced expansions and fixation in the domesticated silkworm but not in wild silkworm. Furthermore, the ML results indicated that purifying selection of TEs in the domesticated silkworm were significantly weaker than that in the wild silkworm. Interestingly, an adaptation insertion induced by BmMITE-2 was found, and this insertion can reduce the polymorphism of the flanking regions of its neighboring COQ7 gene. Our results suggested that TEs expanded and were fixed in the domesticated silkworm might result from demographic effects and artificial selection during domestication. We concluded that the data presented in this study have general implication in animal and crop improvements as well as in domestication of new species.     

A brief history of the status of transposable elements: from junk DNA to major players in evolution

The idea that some genetic factors are able to move around chromosomes emerged more than 60 years ago when Barbara McClintock first suggested that such elements existed and had a major role in controlling gene expression and that they also have had a major influence in reshaping genomes in evolution. It was many years, however, before the accumulation of data and theories showed that this latter revolutionary idea was correct although, understandably, it fell far short of our present view of the significant influence of what are now known as "transposable elements" in evolution. In this article, I summarize the main events that influenced my thinking about transposable elements as a young scientist and the influence and role of these specific genomic elements in evolution over subsequent years. Today, we recognize that the findings about genomic changes affected by transposable elements have considerably altered our view of the ways in which genomes evolve and work.     

Colonization of heterochromatic genes by transposable elements in Drosophila

As a further step toward understanding transposable element-host genome interactions, we investigated the molecular anatomy of introns from five heterochromatic and 22 euchromatic protein-coding genes of Drosophila melanogaster. A total of 79 kb of intronic sequences from heterochromatic genes and 355 kb of intronic sequences from euchromatic genes have been used in Blast searches against Drosophila transposable elements (TEs). The results show that TE-homologous sequences belonging to 19 different families represent about 50% of intronic DNA from heterochromatic genes. In contrast, only 0.1% of the euchromatic intron DNA exhibits homology to known TEs. Intraspecific and interspecific size polymorphisms of introns were found, which are likely to be associated with changes in TE-related sequences. Together, the enrichment in TEs and the apparent dynamic state of heterochromatic introns suggest that TEs contribute significantly to the evolution of genes located in heterochromatin.     

Mavericks, a novel class of giant transposable elements widespread in eukaryotes and related to DNA viruses

We previously identified a group of atypical mobile elements designated Mavericks from the nematodes Caenorhabditis elegans and C. briggsae and the zebrafish Danio rerio. Here we present the results of comprehensive database searches of the genome sequences available, which reveal that Mavericks are widespread in invertebrates and non-mammalian vertebrates but show a patchy distribution in non-animal species, being present in the fungi Glomus intraradices and Phakopsora pachyrhizi and in several single-celled eukaryotes such as the ciliate Tetrahymena thermophila, the stramenopile Phytophthora infestans and the trichomonad Trichomonas vaginalis, but not detectable in plants. This distribution, together with comparative and phylogenetic analyses of Maverick-encoded proteins, is suggestive of an ancient origin of these elements in eukaryotes followed by lineage-specific losses and/or recurrent episodes of horizontal transmission. In addition, we report that Maverick elements have amplified recently to high copy numbers in T. vaginalis where they now occupy as much as 30% of the genome. Sequence analysis confirms that most Mavericks encode a retroviral-like integrase, but lack other open reading frames typically found in retroelements. Nevertheless, the length and conservation of the target site duplication created upon Maverick insertion (5- or 6-bp) is consistent with a role of the integrase-like protein in the integration of a double-stranded DNA transposition intermediate. Mavericks also display long terminal-inverted repeats but do not contain ORFs similar to proteins encoded by DNA transposons. Instead, Mavericks encode a conserved set of 5 to 9 genes (in addition to the integrase) that are predicted to encode proteins with homology to replication and packaging proteins of some bacteriophages and diverse eukaryotic double-stranded DNA viruses, including a DNA polymerase B homolog and putative capsid proteins. Based on these and other structural similarities, we speculate that Mavericks represent an evolutionary missing link between seemingly disparate invasive DNA elements that include bacteriophages, adenoviruses and eukaryotic linear plasmids.     

Birth and death of genes promoted by transposable elements in Oryza sativa

Despite a wide distribution of transposable elements (TEs) in the genomes of higher eukaryotes, much of their evolutionary significance remains unclear. Recent studies have indicated that TEs are involved with biological processes such as gene regulation and the generation of new exons in mammals. In addition, the completion of the genome sequencings in Arabidopsis thaliana and Oryza sativa has permitted scientist to describe a genome-wide overview in plants. In this study, we examined the positions of TEs in the genome of O. sativa. Although we found that more than 10% of the structural genes contained TEs, they were underrepresented in exons compared with non-exonic regions. TEs also appeared to be inserted preferentially in 3'-untranslated regions in exons. These results suggested that purifying selection against TE insertion has played a major role during evolution. Moreover, our comparison of the numbers of TEs in the protein-coding regions between single copy genes and duplicate genes showed that TEs were more frequent in duplicate than single copy genes. This observation indicated that gene duplication events created a large number of functionally redundant genes. Subsequently, many of them were destroyed by TEs because the redundant copies were released from purifying selection. Another biological role of TEs was found to be the recruitment of new exons. We found that approximately 2% of protein-coding genes contained TEs in their coding regions. Insertion of TEs in genic regions may have the potential to be an evolutionary driving force for the creation of new biological functions.     

Mrs, a new subfamily of Tourist transposable elements

We have characterised a new family of repetitive sequences that we have named Mrs (maize repetitive sequences). Mrs elements are associated with different maize genes and seem to be specific for the genome of Zea species. Mrs elements are short, AT-rich and contain terminal inverted repeats (TIRs). The sequence of their TIRs, as well as the fact that they are flanked by short repetitions that tend to be TAA, allows us to propose Mrs as a new subfamily of Tourist transposable elements.     

Turning genes off by Ssn6-Tup1: a conserved system of transcriptional repression in eukaryotes

The Ssn6-Tup1 repressor forms one of the largest and most important gene-regulatory circuits in budding yeast. This circuit, which appears conserved in flies, worms and mammals, exemplifies how a 'global' repressor (i.e. a repressor that regulates many genes in the cell) can be highly selective in the genes it represses. It also explains how, given the appropriate signal, specific subsets of these genes can be derepressed. Ssn6-Tup1 seems especially robust, bringing about a high level of repression irrespective of its precise placement on DNA or of specific features of the DNA control regions of its target genes. This high degree of repression probably results from several distinct mechanisms acting together.     

A family of human microRNA genes from miniature inverted-repeat transposable elements

While hundreds of novel microRNA (miRNA) genes have been discovered in the last few years alone, the origin and evolution of these non-coding regulatory sequences remain largely obscure. In this report, we demonstrate that members of a recently discovered family of human miRNA genes, hsa-mir-548, are derived from Made1 transposable elements. Made1 elements are short miniature inverted-repeat transposable elements (MITEs), which consist of two 37 base pair (bp) terminal inverted repeats that flank 6 bp of internal sequence. Thus, Made1 elements are nearly perfect palindromes, and when expressed as RNA they form highly stable hairpin loops. Apparently, these Made1-related structures are recognized by the RNA interference enzymatic machinery and processed to form 22 bp mature miRNA sequences. Consistent with their origin from MITEs, hsa-mir-548 genes are primate-specific and have many potential paralogs in the human genome. There are more than 3,500 putative hsa-mir-548 target genes; analysis of their expression profiles and functional affinities suggests cancer-related regulatory roles for hsa-mir-548. Taken together, the characteristics of Made1 elements, and MITEs in general, point to a specific mechanism for the generation of numerous small regulatory RNAs and target sites throughout the genome. The evolutionary lineage-specific nature of MITEs could also provide for the generation of novel regulatory phenotypes related to species diversification. Finally, we propose that MITEs may represent an evolutionary link between siRNAs and miRNAs.     

Mavericks, a novel class of giant transposable elements widespread in eukaryotes and related to DNA viruses

We previously identified a group of atypical mobile elements designated Mavericks from the nematodes Caenorhabditis elegans and C. briggsae and the zebrafish Danio rerio. Here we present the results of comprehensive database searches of the genome sequences available, which reveal that Mavericks are widespread in invertebrates and non-mammalian vertebrates but show a patchy distribution in non-animal species, being present in the fungi Glomus intraradices and Phakopsora pachyrhizi and in several single-celled eukaryotes such as the ciliate Tetrahymena thermophila, the stramenopile Phytophthora infestans and the trichomonad Trichomonas vaginalis, but not detectable in plants. This distribution, together with comparative and phylogenetic analyses of Maverick-encoded proteins, is suggestive of an ancient origin of these elements in eukaryotes followed by lineage-specific losses and/or recurrent episodes of horizontal transmission. In addition, we report that Maverick elements have amplified recently to high copy numbers in T. vaginalis where they now occupy as much as 30% of the genome. Sequence analysis confirms that most Mavericks encode a retroviral-like integrase, but lack other open reading frames typically found in retroelements. Nevertheless, the length and conservation of the target site duplication created upon Maverick insertion (5- or 6-bp) is consistent with a role of the integrase-like protein in the integration of a double-stranded DNA transposition intermediate. Mavericks also display long terminal-inverted repeats but do not contain ORFs similar to proteins encoded by DNA transposons. Instead, Mavericks encode a conserved set of 5 to 9 genes (in addition to the integrase) that are predicted to encode proteins with homology to replication and packaging proteins of some bacteriophages and diverse eukaryotic double-stranded DNA viruses, including a DNA polymerase B homolog and putative capsid proteins. Based on these and other structural similarities, we speculate that Mavericks represent an evolutionary missing link between seemingly disparate invasive DNA elements that include bacteriophages, adenoviruses and eukaryotic linear plasmids.     

Turning text into research networks: information retrieval and computational ontologies in the creation of scientific databases

Background

Web-based, free-text documents on science and technology have been increasing growing on the web. However, most of these documents are not immediately processable by computers slowing down the acquisition of useful information. Computational ontologies might represent a possible solution by enabling semantically machine readable data sets. But, the process of ontology creation, instantiation and maintenance is still based on manual methodologies and thus time and cost intensive.

Method

We focused on a large corpus containing information on researchers, research fields, and institutions. We based our strategy on traditional entity recognition, social computing and correlation. We devised a semi automatic approach for the recognition, correlation and extraction of named entities and relations from textual documents which are then used to create, instantiate, and maintain an ontology.

Results

We present a prototype demonstrating the applicability of the proposed strategy, along with a case study describing how direct and indirect relations can be extracted from academic and professional activities registered in a database of curriculum vitae in free-text format. We present evidence that this system can identify entities to assist in the process of knowledge extraction and representation to support ontology maintenance. We also demonstrate the extraction of relationships among ontology classes and their instances.

Conclusion

We have demonstrated that our system can be used for the conversion of research information in free text format into database with a semantic structure. Future studies should test this system using the growing number of free-text information available at the institutional and national levels.     

Internal deletions of transposable elements: the case of Lemi elements

Mobile elements using a “cut and paste” mechanism of transposition (Class II) are frequently prone to internal deletions and the question of the origin of these copies remains elusive. In this study, we looked for copies belonging to the Lemi Family (Tc1-mariner-IS630 SuperFamily) in the plant genomes, and copies within internal deletions were analyzed in detail. Lemi elements are found exclusively in Eudicots, and more than half of the copies have been deleted. All deletions occur between microhomologies (direct repeats from 2 to 13 bp). Copies less than 500 bp long, similar to MITEs, are frequent. These copies seem to result from large deletions occurring between microhomologies present within a region of 300 bp at both extremities of the element. These regions are particularly A/T rich, compared to the internal part of the element, which increases the probability of observing short direct repeats. Most of the molecular mechanisms responsible for double strand break repair are able to induce deletions between microhomologies during the repair process. This could be a quick way to reduce the population of active copies within a genome and, more generally, to reduce the overall activity of the element after it has entered a naive genome.     

Revising the selfish DNA hypothesis: new evidence on accumulation of transposable elements in heterochromatin

The bulk of the eukaryotic genome is composed of families of repetitive sequences that are genetically silent and exhibit various types of instability. Transposable elements (TEs) are particularly common in heterochromatic regions of the genome - a location where TEs might do less damage to their host. Recent advances suggest that the relationship between TEs and heterochromatin might not be quite so straightforward.