Transposable elements and the evolution of eukaryotic complexity

Eukaryotic transposable elements are ubiquitous and widespread mobile genetic entities. These elements often make up a substantial fraction of the host genomes in which they reside. For example, approximately 1/2 of the human genome was recently shown to consist of transposable element sequences. There is a growing body of evidence that demonstrates that transposable elements have been major players in genome evolution. A sample of this evidence is reviewed here with an emphasis on the role that transposable elements may have played in driving the evolution of eukaryotic complexity. A number of specific scenarios are presented that implicate transposable elements in the evolution of the complex molecular and cellular machinery that are characteristic of the eukaryotic domain of life.     

Effects of recombination rate on human endogenous retrovirus fixation and persistence

Endogenous retroviruses (ERVs) result from germ line infections by exogenous retroviruses. They can proliferate within the genome of their host species until they are either inactivated by mutation or removed by recombinational deletion. ERVs belong to a diverse group of mobile genetic elements collectively termed transposable elements (TEs). Numerous studies have attempted to elucidate the factors determining the genomic distribution and persistence of TEs. Here we show that, within humans, gene density and not recombination rate correlates with fixation of endogenous retroviruses, whereas the local recombination rate determines their persistence in a full-length state. Recombination does not appear to influence fixation either via the ectopic exchange model or by indirect models based on the efficacy of selection. We propose a model linking rates of meiotic recombination to the probability of recombinational deletion to explain the effect of recombination rate on persistence. Chromosomes 19 and Y are exceptions, possessing more elements than other regions, and we suggest this is due to low gene density and elevated rates of human ERV integration in males for chromosome Y and segmental duplication for chromosome 19.     

Transposable elements and the evolution of genome organization in mammals

All mammalian transposable elements characterized to date appear to be nonrandomly distributed in the mammalian genome. While no element has been found to be exclusively restricted in its chromosomal location, LINE elements and some retrovirus-like elements are preferentially accumulated in G-banding regions of the chromosomes, and in some cases in the sex chromosomes, while SINE elements occur preferentially in R-banding regions. Four mechanisms are presented which may explain the nonrandom genomic distribution of mammalian transposons: i) sequence-specific insertion, ii) S-phase insertion, iii) ectopic excision, and iv) recombinational editing. Some of the available data are consistent with each of these four models, but no single model is sufficient to explain all of the existing data.     

Modular structure of the genes of phages-transposons of Pseudomonas aeruginosa

The basic criterion to confirm the recombinational origin of bacteriophages belonging to the same phage family is revealing several different combinations of differentiated segments in phage genomes which determine specific functions (modules). The results of phage-to-phage comparison of several regions in genomes of closely related transposable phages of Pseudomonas aeruginosa D3112, B39, PH2, PH51, PH93, PH132 have supported the modular hypothesis for this group of phages.     

Transposable elements as artisans of the heterochromatic genome in Drosophila melanogaster

Over 50 years ago Barbara McClintock discovered that maize contains mobile genetic elements, but her findings were at first considered nothing more than anomalies. Today it is widely recognized that transposable elements have colonized all eukaryotic genomes and represent a major force driving evolution of organisms. Our contribution to this special issue deals with the theme of transposable element-host genome interactions. We bring together published and unpublished work to provide a picture of the contribution of transposable elements to the evolution of the heterochromatic genome in Drosophila melanogaster. In particular, we discuss data on 1) colonization of constitutive heterochromatin by transposable elements, 2) instability of constitutive heterochromatin induced by the I factor, and 3) evolution of constitutive heterochromatin and heterochromatic genes driven by transposable elements. Drawing attention to these topics may have direct implications on important aspects of genome organization and gene expression.     

原生动物基因组转座元件的研究进展

转座元件是一类广泛分布于真核生物的可移动的遗传因子, 可以引起基因重组和变异, 在物种进化及遗传改良中起着重要作用。针对近年来原生动物全基因组序列中大量发现的转座元件, 文章着重比较了转座元件在锥虫、利什曼虫、微孢子虫、变形虫和滴虫基因组序列中的存在种类、分布特征及其功能意义。原生动物转座元件以LINE 和SINE为主, 其次是DNA转座元件和LTR反转座元件, 部分转座元件在高A+T含量区富集, 预示着转座元件与基因组序列A+T含量有着紧密联系。根据不同种微孢子虫基因组之间转座元件的差异, 推测在微孢子虫基因组进化过程中, 至少经历了一次转座元件的丢失事件。最后对转座元件在原生动物寄生虫的进一步研究和应用作了展望。     

果蝇转座因子对基因组进化的影响

真核生物基因组织有很多可移动ＤＮＡ片段为称转座因子,果蝇是大量系统研究的最好实验材料之一,其基因组的１０％－１２％是由转座因子组成,在宿主中,ＴＥs也许改变基因表达模型,也许改变ＯＲＦs编码序列,也许对细胞功能产生影响,这此因子遗传的可动性也可能使它们适于建造载体产生转基因生物。因此,对ＴＥs进化的动态研究以及对宿主基因组进化影响的探索将有助于TEs作为载体的细胞工程研究。     

Recent amplification of the kangaroo endogenous retrovirus, KERV, limited to the centromere

Mammalian retrotransposons, transposable elements that are processed through an RNA intermediate, are categorized as short interspersed elements (SINEs), long interspersed elements (LINEs), and long terminal repeat (LTR) retroelements, which include endogenous retroviruses. The ability of transposable elements to autonomously amplify led to their initial characterization as selfish or junk DNA; however, it is now known that they may acquire specific cellular functions in a genome and are implicated in host defense mechanisms as well as in genome evolution. Interactions between classes of transposable elements may exert a markedly different and potentially more significant effect on a genome than interactions between members of a single class of transposable elements. We examined the genomic structure and evolution of the kangaroo endogenous retrovirus (KERV) in the marsupial genus Macropus. The complete proviral structure of the kangaroo endogenous retrovirus, phylogenetic relationship among relative retroviruses, and expression of this virus in both Macropus rufogriseus and M. eugenii are presented for the first time. In addition, we show the relative copy number and distribution of the kangaroo endogenous retrovirus in the Macropus genus. Our data indicate that amplification of the kangaroo endogenous retrovirus occurred in a lineage-specific fashion, is restricted to the centromeres, and is not correlated with LINE depletion. Finally, analysis of KERV long terminal repeat sequences using massively parallel sequencing indicates that the recent amplification in M. rufogriseus is likely due to duplications and concerted evolution rather than a high number of independent insertion events.     

Evolution of transposable elements: an IS10 insertion increases fitness in Escherichia coli

Strains of Escherichia coli carrying Tn10, a transposon consisting of two IS10 insertion sequences flanking a segment encoding for a tetracycline-resistance determinant, gain a competitive advantage in chemostat cultures. All Tn10-bearing strains that increase in frequency during competition have a new IS10 insertion that is found in the same location in the genome of those strains. We mapped, by a gradient of transmission, the position of the new IS10 insertion. We examined 11 isolates whose IS10 insertion was deleted by recombinational crossing- over, and in all cases the competitive fitness of the isolates was decreased. These results show that the IS10-generated insertion increases fitness in chemostat cultures. We named the insertion fit::IS10 and suggest that transposable elements may speed the rate of evolution by promoting nonhomologous recombination between preexisting variations within a genome and thereby generating adaptive variation.      

Somatic excision of the Mu1 transposable element of maize.

The Mu transposons of the Robertsons's Mutator transposable element system in maize are unusual in many respects, when compared to the other known plant transposon systems. The excision of these elements occurs late in somatic tissues and very rarely in the germ line. Unlike the other plant transposons, there is no experimental evidence directly linking Mu element excision and integration. We have analyzed the excision products generated by a Mu1 transposon inserted into the bronze 1 locus of maize. We find that the excision products or 'footprints' left by the Mu1 element resemble those of the other plant transposable elements, rather than those of the animal transposable element systems. We also find some novel types of footprints resembling recombinational events. We suggest that the Mu1 element can promote intrachromosomal crossovers and conversions near its site of insertion, and that this may be another mechanism by which transposons can accelerate the evolution of genomes.     

Role of transposable elements in trypanosomatids

Transposable elements constitute 2-5% of the genome content in trypanosomatid parasites. Some of them are involved in critical cellular functions, such as the regulation of gene expression in Leishmania spp. In this review, we highlight the remarkable role extinct transposable elements can play as the source of potential new functions.     

Survey of transposable elements from rice genomic sequences

Oryza sativa L. (domesticated rice) is a monocotyledonous plant, and its 430 Mb genome has been targeted for complete sequencing. We performed a high-resolution computer-based survey for transposable elements on 910 Kb of rice genomic DNA sequences. Both class I and II transposable elements were present, contributing 19.9% of the sequences surveyed. Class II elements greatly outnumbered class I elements (166 versus 22), although class I elements made up a greater percentage (12.2% versus 6.6%) of nucleotides surveyed. Several Mutator-like elements (MULEs) were identified, including rice elements that harbor truncated host cellular genes. MITEs (miniature inverted-repeat transposable elements) account for 71.6% of the mined transposable elements and are clearly the predominant type of transposable element in the sequences examined. Moreover, a putative Stowaway transposase has been identified based on shared sequence similarity with the mined MITEs and previously identified plant mariner-like elements (MLEs). Members of a group of novel rice elements resembling the structurally unusual members of the Basho family in Arabidopsis suggest a wide distribution of these transposons among plants. Our survey provides a preview of transposable element diversity and abundance in rice, and allows for comparison with genomes of other plant species.     

Selected translocation of plasmid genes: frequency and regional specificity of translocation of the Tn3 element.

A procedure is described that selects for the insertion of transposable antibiotic resistance elements in a variety of recipient replicons. The selected translocation procedure, which employs a plasmid having a temperature-sensitive defect in replication as a donor of transposable genetic elements, was used to investigate certain characteristics of the translocation process. Our results indicate that translocation of the Tn3 element from plasmid to plasmid occurs at a 10(3)- to 10(4)-times-higher frequency than from plasmid to chromosome. In both cases, continued accumulation of Tn3 on recipient genomes is prevented by development of an apparent equilibrium when only a small fraction of molecules in the recipient population contain Tn3. An alternative method for estimation of translocation frequency has shown that the translocation process is temperature sensitive and that its frequency is unaffected by the presence of host recA mutation. Insertions of Tn3 onto the 65 X 10(6)-dalton R6-5 plasmid in Escherichia coli are clustered on EcoRI fragments 3 (8 of 23 insertions) and 9 (7 of 23 insertions), which contain 12 and 5%, respectively, of the R6-5 genome. The occurrence of multiple insertions of Tn3 within EcoRI fragment 9, which contains the IS1 element and a terminus of the Tn4 element, is consistent with earlier evidence indicating that terminal deoxyribonucleic acid sequences of already present transposable elements may provide recognition sequences for subsequent illegitimate recombinational events.     

Transposon excision from an atypical site: a mechanism of evolution of novel transposable elements

The role of transposable elements in sculpting the genome is well appreciated but remains poorly understood. Some organisms, such as humans, do not have active transposons; however, transposable elements were presumably active in their ancestral genomes. Of specific interest is whether the DNA surrounding the sites of transposon excision become recombinogenic, thus bringing about homologous recombination. Previous studies in maize and Drosophila have provided conflicting evidence on whether transposon excision is correlated with homologous recombination. Here we take advantage of an atypical Dissociation (Ds) element, a maize transposon that can be mobilized by the Ac transposase gene in Arabidopsis thaliana, to address questions on the mechanism of Ds excision. This atypical Ds element contains an adjacent 598 base pairs (bp) inverted repeat; the element was allowed to excise by the introduction of an unlinked Ac transposase source through mating. Footprints at the excision site suggest a micro-homology mediated non-homologous end joining reminiscent of V(D)J recombination involving the formation of intra-helix 3' to 5' trans-esterification as an intermediate, a mechanism consistent with previous observations in maize, Antirrhinum and in certain insects. The proposed mechanism suggests that the broken chromosome at the excision site should not allow recombinational interaction with the homologous chromosome, and that the linked inverted repeat should also be mobilizable. To test the first prediction, we measured recombination of flanking chromosomal arms selected for the excision of Ds. In congruence with the model, Ds excision did not influence crossover recombination. Furthermore, evidence for correlated movement of the adjacent inverted repeat sequence is presented; its origin and movement suggest a novel mechanism for the evolution of repeated elements. Taken together these results suggest that the movement of transposable elements themselves may not directly influence linkage. Possibility remains, however, for novel repeated DNA sequences produced as a consequence of transposon movement to influence crossover in subsequent generations.     

An abundant family of methylated repetitive sequences dominates the genome of Physarum polycephalum.

A significant portion (20%) of the Physarum genome can be isolated as a HpaII-resistant, methylated fraction. Cloned DNA probes containing highly-repeated sequences derived from this fraction were used to define the pattern of structural organisation of homologous repeats in Physarum genomic DNA. It is shown that the probes detect an abundant, methylated family of sequences with an estimated genomic repetition frequency greater than 2100, derived from a large repeated element whose length exceeds 5.8kb. Sequences comprising the long repetitive element dominate the HpaII-resistant compartment and account for between 4-20% of the Physarum genome. Detailed restriction/hybridisation analysis of cloned DNA segments derived from this compartment shows that HpaII/MspI restriction sites within some copies of the long repeated sequence are probably deleted by mutation. Additionally, segments of the repeat are often found in different organisational patterns that represent scrambled versions of its basic structure, and which are presumed to have arisen as a result of recombinational rearrangement in situ in the Physarum genome. Preliminary experiments indicate that the sequences are transcribed and that the structural properties of the repeat bear some resemblance to those of transposable genetic elements defined in other eukaryotic species.     

Mechanisms regulating the copy numbers of six LTR retrotransposons in the genome of Drosophila melanogaster

There has been debate over the mechanisms that control the copy number of transposable elements in the genome of Drosophila melanogaster. Target sites in D. melanogaster populations are occupied at low frequencies, suggesting that there is some form of selection acting against transposable elements. Three main theories have been proposed to explain how selection acts against transposable elements: insertions of a copy of a transposable element are selected against; chromosomal rearrangements caused by ectopic exchange between element copies are selected against; or the process of transposition itself is selected against. The three theories give different predictions for the pattern of transposable element insertions in the chromosomes of D. melanogaster. We analysed the abundance of six LTR (long terminal repeat) retrotransposons on the X and fourth chromosomes of multiple strains of D. melanogaster, which we compare with the predictions of each theory. The data suggest that no one theory can account for the insertion patterns of all six retrotransposons. Comparing our results with earlier work using these transposable element families, we find a significant correlation between studies in the particular model of copy number regulation supported by the proportion of elements on the X for the different transposable element families. This suggests that different retrotransposon families are regulated by different mechanisms.     

Evolution and Extinction of Transposable Elements in Mendelian Populations

A model of the evolution of a transposable element family in a Mendelian host population is proposed that incorporates heritable phenotypic mutations in the elements. The temporal behavior of the numbers of mutant and wild-type elements is studied, and the expected extinction time of the transposable element family is examined. Our results indicate that, if the mutant can be transposed equally well in the presence of the wild type, then it can be expected to be found in preponderance, whereas elements, such as retroviruses, where the transposing genome and its phenotypic expression are coupled, may be characterized by a low mutant frequency.