Transposable elements in the Animal Kingdom

Transposable elements (TEs) are commonly thought to be of universal occurrence in eukaryotes. Analysis of complete higher eukaryotic genomes confirms TE status as substantial genome components and provides insights into their role in shaping the genome structure of extant eukaryotes. This review addresses several recently investigated problems in transposon biology, including potential roles of promoter organization in transposon function and evolution, the ubiquity of TEs in numerous phyla of the animal kingdom, and possible connections between transposon content and the mode of reproduction.     

Wake up of transposable elements following Drosophila simulans worldwide colonization.

Transposable elements (TEs) make up around 10%-15% of the Drosophila melanogaster genome, but its sibling species Drosophila simulans carries only one third as many such repeat sequences. We do not, however, have an overall view of copy numbers of the various classes of TEs (long terminal repeat [LTR] retrotransposons, non-LTR retrotransposons, and transposons) in genomes of natural populations of both species. We analyzed 34 elements in individuals from various natural populations of these species. We show that D. melanogaster has higher average chromosomal insertion site numbers per genome than D. simulans for all TEs except five. The LTR retrotransposons gypsy, ZAM, and 1731 and the transposon bari-1 present similar low copy numbers in both species. The transposon hobo has a large number of insertion sites, with significantly more sites in D. simulans. High variation between populations in number of insertion sites of some elements of D. simulans suggests that these elements can invade the genome of the entire species starting from a local population. We propose that TEs in the D. simulans genome are being awakened and amplified as they had been a long time ago in D. melanogaster.     

Mobilization of Stowaway-like MITEs in newly formed allohexaploid wheat species

Transposable elements (TEs) dominate the genetic capacity of most eukaryotes, especially plants, where they can account for up to 90?% of the genome, such as in wheat. The relationship between TEs and their hosts and the role of TEs in organismal biology are poorly understood. In this study, we have applied next generation sequencing, together with a transposon display technique in order to test whether a Stowaway-like MITE, termed Minos, transposes following allopolyploidization events in wheat. We have generated a 454-pyrosequencing database of Minos-specific amplicons (transposon display products) from a newly formed wheat allohexaploid and its parental lines and retrieved hundreds of novel MITE insertions in the allohexaploid. Clear mobilization of Minos was also seen by site-specific PCR analysis and sequence validation. In addition, using real-time qPCR analysis we observed an insignificant change in the relative quantity of Minos from the expected value of merging the two parental genomes, indicating that, despite its activation, no significant burst in Minos copy number can be seen in the newly formed allohexaploid. Interestingly, we found that CCGG sites surrounding Minos underwent massive hypermethylation following the allohexaploidization process. Our data suggest that MITEs have maintained their capacity for activity throughout the evolution of wheat and might be epigenetically deregulated in the first generations following allopolyploidization.     

DNA methylome analysis provides evidence that the expansion of the tea genome is linked to TE bursts

DNA methylation is essential for gene regulation, imprinting and silencing of transposable elements (TEs). Although bursts of transposable elements are common in many plant lineages, how plant DNA methylation is related to transposon bursts remains unclear. Here we explore the landscape of DNA methylation of tea, a species thought to have experienced a recent transposon burst event. This species possesses more transposable elements than any other sequenced asterids (potato, tomato, coffee, pepper and tobacco). The overall average DNA methylation levels were found to differ among the tea, potato and tomato genomes, and methylation at CHG sequence sites was found to be significantly higher in tea than that in potato or tomato. Moreover, the abundant TEs resulting from burst events not only resulted in tea developing a very large genome size, but also affected many genes involved in importantly biological processes, including caffeine, theanine and flavonoid metabolic pathway genes. In addition, recently transposed TEs were more heavily methylated than ancient ones, implying that DNA methylation is proportionate to the degree of TE silencing, especially on recent active ones. Taken together, our results show that DNA methylation regulates transposon silencing and may play a role in genome size expansion.     

Fish transposons and their potential use in aquaculture

A large part of repetitive DNA of vertebrate genomes have been identified as transposon elements (TEs) or mobile sequences. Although TEs detected to date in most vertebrates are inactivated, active TEs have been found in fish and a salmonid TE has been successfully reactivated by molecular genetic manipulation from inactive genomic copies (Sleeping Beauty, SB). Progress in the understanding of the dynamics, control and evolution of fish TEs will allow the insertion of selected sequences into the fish genomes of germ cells to obtain transgenics or to identify genes important for growth and/or of somatic cells to improve DNA vaccination. Expectations are high for new possible applications to fish of this well developed technology for mammals. Here, we review the present state of knowledge of inactive and active fish TEs and briefly discuss how their possible future applications might be used to improve fish production in aquaculture.     

Transposable Elements Cross Kingdom Boundaries and Contribute to Inflammation and Ageing

The de-repression of transposable elements (TEs) in mammalian genomes is thought to contribute to genome instability, inflammation, and ageing, yet is viewed as a cell-autonomous event. In contrast to mammalian cells, prokaryotes constantly exchange genetic material through TEs, crossing both cell and species barriers, contributing to rapid microbial evolution and diversity in complex communities such as the mammalian gut. Here, it is proposed that TEs released from prokaryotes in the microbiome or from pathogenic infections regularly cross the kingdom barrier to the somatic cells of their eukaryotic hosts. It is proposed this horizontal transfer of TEs from microbe to host is a stochastic, ongoing catalyst of genome destabilization, resulting in structural and epigenetic variations, and activation of well-evolved host defense mechanisms contributing to inflammation, senescence, and biological ageing. It is proposed that innate immunity pathways defend against the horizontal acquisition of microbial TEs, and that activation of this pathway during horizontal transposon transfer promotes chronic inflammation during ageing. Finally, it is suggested that horizontal acquisition of prokaryotic TEs into mammalian genomes has been masked and subsequently under-reported due to flaws in current sequencing pipelines, and new strategies to uncover these events are proposed.     

Next-generation sequencing reveals recent horizontal transfer of a DNA transposon between divergent mosquitoes

Horizontal transfer of genetic material between complex organisms often involves transposable elements (TEs). For example, a DNA transposon mariner has been shown to undergo horizontal transfer between different orders of insects and between different phyla of animals. Here we report the discovery and characterization of an ITmD37D transposon, MJ1, in Anopheles sinensis. We show that some MJ1 elements in Aedes aegypti and An. sinensis contain intact open reading frames and share nearly 99% nucleotide identity over the entire transposon, which is unexpectedly high given that these two genera had diverged 145-200 million years ago. Chromosomal hybridization and TE-display showed that MJ1 copy number is low in An. sinensis. Among 24 mosquito species surveyed, MJ1 is only found in Ae. aegypti and the hyrcanus group of anopheline mosquitoes to which An. sinensis belongs. Phylogenetic analysis is consistent with horizontal transfer and provides the basis for inference of its timing and direction. Although report of horizontal transfer of DNA transposons between higher eukaryotes is accumulating, our analysis is one of a small number of cases in which horizontal transfer of nearly identical TEs among highly divergent species has been thoroughly investigated and strongly supported. Horizontal transfer involving mosquitoes is of particular interest because there are ongoing investigations of the possibility of spreading pathogen-resistant genes into mosquito populations to control malaria and other infectious diseases. The initial indication of horizontal transfer of MJ1 came from comparisons between a 0.4x coverage An. sinensis 454 sequence database and available TEs in mosquito genomes. Therefore we have shown that it is feasible to use low coverage sequencing to systematically uncover horizontal transfer events. Expanding such efforts across a wide range of species will generate novel insights into the relative frequency of horizontal transfer of different TEs and provide the evolutionary context of these lateral transfer events.     

Mating system shifts and transposable element evolution in the plant genus Capsella

Background

Despite having predominately deleterious fitness effects, transposable elements (TEs) are major constituents of eukaryote genomes in general and of plant genomes in particular. Although the proportion of the genome made up of TEs varies at least four-fold across plants, the relative importance of the evolutionary forces shaping variation in TE abundance and distributions across taxa remains unclear. Under several theoretical models, mating system plays an important role in governing the evolutionary dynamics of TEs. Here, we use the recently sequenced Capsella rubella reference genome and short-read whole genome sequencing of multiple individuals to quantify abundance, genome distributions, and population frequencies of TEs in three recently diverged species of differing mating system, two self-compatible species (C. rubella and C. orientalis) and their self-incompatible outcrossing relative, C. grandiflora.

Results

We detect different dynamics of TE evolution in our two self-compatible species; C. rubella shows a small increase in transposon copy number, while C. orientalis shows a substantial decrease relative to C. grandiflora. The direction of this change in copy number is genome wide and consistent across transposon classes. For insertions near genes, however, we detect the highest abundances in C. grandiflora. Finally, we also find differences in the population frequency distributions across the three species.

Conclusion

Overall, our results suggest that the evolution of selfing may have different effects on TE evolution on a short and on a long timescale. Moreover, cross-species comparisons of transposon abundance are sensitive to reference genome bias, and efforts to control for this bias are key when making comparisons across species.

Electronic supplementary material

The online version of this article (doi:10.1186/1471-2164-15-602) contains supplementary material, which is available to authorized users.     

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.     

Transposable Elements as Stress Adaptive Capacitors Induce Genomic Instability in Fungal Pathogen Magnaporthe oryzae

A fundamental problem in fungal pathogenesis is to elucidate the evolutionary forces responsible for genomic rearrangements leading to races with fitter genotypes. Understanding the adaptive evolutionary mechanisms requires identification of genomic components and environmental factors reshaping the genome of fungal pathogens to adapt. Herein, Magnaporthe oryzae, a model fungal plant pathogen is used to demonstrate the impact of environmental cues on transposable elements (TE) based genome dynamics. For heat shock and copper stress exposed samples, eight TEs belonging to class I and II family were employed to obtain DNA profiles. Stress induced mutant bands showed a positive correlation with dose/duration of stress and provided evidences of TEs role in stress adaptiveness. Further, we demonstrate that genome dynamics differ for the type/family of TEs upon stress exposition and previous reports of stress induced MAGGY transposition has underestimated the role of TEs in M. oryzae. Here, we identified Pyret, MAGGY, Pot3, MINE, Mg-SINE, Grasshopper and MGLR3 as contributors of high genomic instability in M. oryzae in respective order. Sequencing of mutated bands led to the identification of LTR-retrotransposon sequences within regulatory regions of psuedogenes. DNA transposon Pot3 was identified in the coding regions of chromatin remodelling protein containing tyrosinase copper-binding and PWWP domains. LTR-retrotransposons Pyret and MAGGY are identified as key components responsible for the high genomic instability and perhaps these TEs are utilized by M. oryzae for its acclimatization to adverse environmental conditions. Our results demonstrate how common field stresses change genome dynamics of pathogen and provide perspective to explore the role of TEs in genome adaptability, signalling network and its impact on the virulence of fungal pathogens.     

Rampant horizontal transfer of SPIN transposons in squamate reptiles

Transposable elements (TEs) are highly abundant in the genome and capable of mobility, two properties that make them particularly prone to transfer horizontally between organisms. Although the impact of horizontal transfer (HT) of TEs is well recognized in prokaryotes, the frequency of this phenomenon and its contribution to genome evolution in eukaryotes remain poorly appreciated. Here, we provide evidence that a DNA transposon called SPIN has colonized the genome of 17 species of reptiles representing nearly every major lineage of squamates, including 14 families of lizards, snakes, and amphisbaenians. Slot blot analyses indicate that SPIN has amplified to high copy numbers in most of these species, ranging from 2,000-28,000 copies per haploid genome. In contrast, we could not detect the presence of SPIN in any of the turtles (seven species from seven families) and crocodiles (four species) examined. Genetic distances between SPIN sequences from species belonging to different squamate families are consistently very low (average = 0.1), considering the deep evolutionary divergence of the families investigated (most are >100 My diverged). Furthermore, these distances fall below interfamilial distances calculated for two genes known to have evolved under strong functional constraint in vertebrates (RAG1, average = 0.24 and C-mos, average = 0.27). These data, combined with phylogenetic analyses, indicate that the widespread distribution of SPIN among squamates is the result of at least 13 independent events of HTs. Molecular dating and paleobiogeographical data suggest that these transfers took place during the last 50 My on at least three different continents (North America, South America and, Africa). Together, these results triple the number of known SPIN transfer events among tetrapods, provide evidence for a previously hypothesized transoceanic movement of SPIN transposons during the Cenozoic, and further underscore the role of HT in the evolution of vertebrate genomes.     

Transposable elements and an epigenetic basis for punctuated equilibria

Evolution is frequently concentrated in bursts of rapid morphological change and speciation followed by long‐term stasis. We propose that this pattern of punctuated equilibria results from an evolutionary tug‐of‐war between host genomes and transposable elements (TEs) mediated through the epigenome. According to this hypothesis, epigenetic regulatory mechanisms (RNA interference, DNA methylation and histone modifications) maintain stasis by suppressing TE mobilization. However, physiological stress, induced by climate change or invasion of new habitats, disrupts epigenetic regulation and unleashes TEs. With their capacity to drive non‐adaptive host evolution, mobilized TEs can restructure the genome and displace populations from adaptive peaks, thus providing an escape from stasis and generating genetic innovations required for rapid diversification. This “epi‐transposon hypothesis” can not only explain macroevolutionary tempo and mode, but may also resolve other long‐standing controversies, such as Wright's shifting balance theory, Mayr's peripheral isolates model, and McClintock's view of genome restructuring as an adaptive response to challenge.     

Correlated evolution of LTR retrotransposons and genome size in the genus <Emphasis Type="Italic">eleocharis</Emphasis>

Background  

Transposable elements (TEs) are considered to be an important source of genome size variation and genetic and phenotypic plasticity in eukaryotes. Most of our knowledge about TEs comes from large genomic projects and studies focused on model organisms. However, TE dynamics among related taxa from natural populations and the role of TEs at the species or supra-species level, where genome size and karyotype evolution are modulated in concert with polyploidy and chromosomal rearrangements, remain poorly understood. We focused on the holokinetic genus Eleocharis (Cyperaceae), which displays large variation in genome size and the occurrence of polyploidy and agmatoploidy/symploidy. We analyzed and quantified the long terminal repeat (LTR) retrotransposons Ty1-copia and Ty3-gypsy in relation to changes in both genome size and karyotype in Eleocharis. We also examined how this relationship is reflected in the phylogeny of Eleocharis.     

Macrotransposition and other complex chromosomal restructuring in maize by closely linked transposons in direct orientation

Several observations indicate that compatible ends of separate, yet closely linked, transposable elements (TEs) can interact in alternative transposition reactions. First, pairs of TEs cause chromosome breaks with frequencies inversely related to the intertransposon distance. Second, some combinations of two TEs produce complex rearrangements that often include DNA adjacent to one or both elements. In pairs of TEs in direct orientation, alternative reactions involving the external ends of the two TEs should lead to the transposition of a macrotransposon consisting of both elements plus the intervening chromosomal segment. Such macrotransposons have been hypothesized previously based on deletions, but no macrotransposon insertions have been recovered. To detect macrotransposition, we have analyzed heritable chromosomal rearrangements produced by a chromosome-breaking pair of Ac and Ds elements situated 6.5 kb apart in direct orientation in a part of the maize (Zea mays) genome dispensable for viability. Here, we show that the postulated macrotransposon can excise and reinsert elsewhere in the genome. In addition, this transposon pair produces other complex rearrangements, including deletions, inversions, and reshuffling of the intertransposon segment. Thus, closely linked TE pairs, a common transposition outcome in some superfamilies, are adept at restructuring chromosomes and may have been instrumental in reshaping plant genomes.     

Constitutive heterochromatin and transposable elements in Drosophila melanogaster

Several families of transposable elements (TEs), most of them belonging to the retrotransposon catagory, are particularly enriched in Drosophila melanogaster constitutive heterochromatin. The enrichment of TE-homologous sequences into heterochromatin is not a peculiar feature of the Drosophila genome, but appears to be widespread among higher eukaryotes. The constitutive heterochromatin of D. melanogaster contains several genetically active domains; this raises the possibility that TE-homologous sequences inserted into functional heterochromatin compartments may be expressed. In this review, I present available data on the genetic and molecular organization of D. melanogaster constitutive heterochromatin and its relationship with transposable elements. The implications of these findings on the possible impact of heterochromatic TEs on the function and evolution of the host genome are also discussed. This revised version was published online in August 2006 with corrections to the Cover Date.     

piRNA抑制基因转座的分子机制

转座子是一类可以在染色体上或不同染色体间自由移动的DNA。在高等生物中,处于活跃状态的转座子多为通过RNA中间体进行转座的逆转录转座子。由于逆转录转座子在细胞基因组中占有很高的比例,它的频繁转座能引起细胞基因组结构和功能的改变,导致癌症等严重基因疾病的发生,因此宿主细胞在长期的进化中形成了多种自我保护机制用以控制逆转录转座子活性。属于非编码小RNA的piRNA以其独特的机制在转录及转录后水平控制逆转录转座子RNA中间体的产生,抑制了逆转录转座过程的发生。本文总结了近年来piRNA控制转座子转座相关分子机制的研究进展,以期为转座子及基因调控方面的研究工作提供一些参考。