The distribution of transposable elements within and between chromosomes in a population of Drosophila melanogaster. I. Element frequencies and distribution.

Data were collected on the distribution of nine families of transposable elements among second and third chromosomes isolated from a natural population of Drosophila melanogaster, by means of in situ hybridization of element probes to polytene chromosomes. It was found that the copy numbers per chromosome in the distal sections of the chromosome arms followed a Poisson distribution. Elements appeared to be distributed randomly along the distal sections of the chromosome arms. There was no evidence for linkage disequilibrium in the distal sections of the chromosomes, but some significant disequilibrium was detected in proximal regions. There were many significant correlations between different element families with respect to the identity of the sites that were occupied in the sample. There were also significant correlations between families with respect to sites at which elements achieved relatively high frequencies. Element frequencies per chromosome band were generally low in the distal sections, but were higher proximally. These results are discussed in the light of models of the population dynamics of transposable elements. It is concluded that they provide strong evidence for the operation of a force or forces opposing transpositional increase in copy number. The data suggest that the rate of transposition per element per generation is of the order of 10(-4), for the elements included in this study.     

Transposable elements in natural populations with a mixture of selected and neutral insertion sites.

This paper examines models of the population dynamics of transposable elements when chromosomal sites vary with respect to the effect on fitness of mutations caused by element insertions. Element abundance is assumed to be stabilised solely by the joint results of transposition, excision, and selection against insertional mutations. When there are only two classes of site, selected and neutral, it is hard to find parameter values for which numbers of elements are maintained that match the findings from surveys of Drosophila populations, as elements tend to accumulate at high frequencies at the neutral sites. It is similarly hard to produce realistic equilibria with three classes of site (strongly selected, weakly selected, and neutral), when elements can transpose out of the neutral sites. If transposition from neutral sites is impossible, as might be the case for elements inserted into centric heterochromatin, then realistic equilibria can be generated if there is very weak selection against elements inserted into the majority of non-neutral sites. This model predicts a modest over-representation of elements at the neutral sites. It also predicts that elements should be under-represented on the X chromosome compared with the autosomes, but this is not generally found to be the case. It is concluded that selection against insertional mutations is unlikely to be the major factor involved in the containment of element abundance.     

A study of ten families of transposable elements on X chromosomes from a population of Drosophila melanogaster

Data were collected on the distribution of ten families of transposable elements among fourteen X chromosomes isolated from a natural population of Drosophila melanogaster, by means of in situ hybridization to polytene chromosomes. It was found that, with the exception of roo, the copy number per chromosome followed a Poisson distribution. There was no evidence for linkage disequilibrium, either within or between families. Some pairs of families of elements were correlated with respect to the identity of the sites that were occupied in the sample, although there was no evidence for a correlation with respect to the sites at which elements attained relatively high frequencies. Elements appeared to be distributed randomly along the distal part of the X chromosome. There was, however, a strong tendency for elements to accumulate at the base of the chromosome. Element frequencies per chromosome band were generally low, except at the base of the chromosome where bands in subdivisions 19E and 20A sometimes had high frequencies of occupation. These results are discussed in the light of models of the population dynamics of transposable elements. It is concluded that they provide strong evidence for the operation of a force or forces opposing transpositional increase in copy number. The accumulation of elements at the base of the chromosome is consistent with the idea that unequal exchange between elements at non-homologous sites is such a force, although other possibilities cannot be excluded at present. The data suggest that the rate of transposition per element per generation is of the order of 10(-4), for the elements included in this study.     

On the abundance and distribution of transposable elements in the genome of Drosophila melanogaster

The abundance and distribution of transposable elements (TEs) in a representative part of the euchromatic genome of Drosophila melanogaster were studied by analyzing the sizes and locations of TEs of all known families in the genomic sequences of chromosomes 2R, X, and 4. TEs contribute to up to 2% of the sequenced DNA, which corresponds roughly to the euchromatin of these chromosomes. This estimate is lower than that previously available from in situ data and suggests that TEs accumulate in the heterochromatin more intensively than was previously thought. We have also found that TEs are not distributed at random in the chromosomes and that their abundance is more strongly associated with local recombination rates, rather than with gene density. The results are compatible with the ectopic exchange model, which proposes that selection against deleterious effects of chromosomal rearrangements is a major force opposing element spread in the genome of this species. Selection against insertional mutations also influences the observed patterns, such as an absence of insertions in coding regions. The results of the analyses are discussed in the light of recent findings on the distribution of TEs in other species.     

Analysis of transposon interruptions suggests selection for L1 elements on the X chromosome

It has been hypothesised that the massive accumulation of L1 transposable elements on the X chromosome is due to their function in X inactivation, and that the accumulation of Alu elements near genes is adaptive. We tested the possible selective advantage of these two transposable element (TE) families with a novel method, interruption analysis. In mammalian genomes, a large number of TEs interrupt other TEs due to the high overall abundance and age of repeats, and these interruptions can be used to test whether TEs are selectively neutral. Interruptions of TEs, which are beneficial for the host, are expected to be deleterious and underrepresented compared with neutral ones. We found that L1 elements in the regions of the X chromosome that contain the majority of the inactivated genes are significantly less frequently interrupted than on the autosomes, while L1s near genes that escape inactivation are interrupted with higher frequency, supporting the hypothesis that L1s on the X chromosome play a role in its inactivation. In addition, we show that TEs are less frequently interrupted in introns than in intergenic regions, probably due to selection against the expansion of introns, but the insertion pattern of Alus is comparable to other repeats.     

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.     

Differential sex chromosome replication and dosage compensation in polytene trichogen cells of Lucilia cuprina (Diptera: Calliphoridae)

Non banded sex chromosome elements have been identified in polytene trichogen cells of Lucilia cuprina using Y-autosome translocations, C-banding and Quinacrine fluorescence. The X chromosome is an irregular granular structure while the much smaller Y chromosome has both a dense darkly stained and a loosely organised segment. The X and Y chromosomes are underreplicated in polytene cells but comparison of C- and Q-banding characteristics of sex chromosomes in diploid and polytene tissues indicates that selective replication of non C-banding material occurs in both the sex chromosomes. Brightly fluorescing material in the Y chromosome is replicated to such an extent that it consists of half the polytene element, while the C-banding material, which makes up most of the diploid X chromosome, is virtually unreplicated. Differential replication also occurs in autosomes. In XXY males, and in males carrying a duplication of the X euchromatic region, a short uniquely banded polytene chromosome is formed. It is suggested that in males carrying two doses of X euchromatin a dosage compensation mechanism operates in which genes in one copy are silenced by forming a banded polytene chromosome.     

Sister chromatid exchange points in the heterochromatin and euchromatin regions of Chinese hedgehog chromosomes

Summary The Chinese hedgehog has a diploid chromosome number of 48 in which there are eleven pairs of telo- or subtelocentric autosomes, twelve pairs of meta- or submetacentric autosomes, a metacentric X chromosome and a telocentric Y chromosome. The heterochromatin is almost completely distributed in five large distal segments of chromosomes nos. 9 to 12 and no. 18. There is no positive C-band in the centromeres of the chromosomes except for the X chromosome which has a small, weakly stained C-band in the centromere. In Chinese hedgehog cells 52.1% of SCEs are found at the junction between the euchromatin and the heterochromatin, 39.5% in the heterochromatin and 8.4% in the auchromatin. The SCE number per unit C-band is double the SCE number per unit euchromatin. The SCE rate in the heterochromatin or euchromatin regions is not proportional to their chromosome length and can be quite different between different pairs of the chromosomes. Our results indicate that there is a non-uniform distribution of the SCEs in the Chinese hedgehog cells.     

Rates of movement of transposable elements on the second chromosome of Drosophila melanogaster

The rates of movement of 11 families of transposable elements of Drosophila melanogaster were studied by means of in situ hybridization of probes to polytene chromosomes of larvae from a long-term mutation accumulation experiment. Replicate mutation-accumulation lines carrying second chromosomes derived from a single common ancestral chromosome were maintained by backcrosses of single males heterozygous for a balancer chromosome and a wild-type chromosome, and were scored after 116 generations. Twenty-seven transpositions and 1 excision were detected using homozygous viable and fertile second chromosomes, for a total of 235,056 potential sources of transposition events and a potential 252,880 excision events. The overall transposition rate per element per generation was 1.15 x 10(-4) and the excision rate was 3.95 x 10(-6). The single excision (of a roo element) was due to recombination between the element's long terminal repeats. A survey of the five most active elements among nine homozygous lethal lines revealed no significant difference in the estimates of transposition and excision rates from those from viable lines. The excess of transposition over excision events is in agreement with the results of other in situ hybridization experiments, and supports the conclusion that replicative increase in transposable element copy number is opposed by selection. These conclusions are compared with those from other studies, and with the conclusions from population surveys of element frequencies.     

Distribution of T1, Q,Pegasus and mariner transposable elements on the polytene chromosomes of PEST,a standard strain of Anopheles gambiae

The chromosomal locations of four families of transposable elements, T1, Q, Pegasus and mariner, have been determined by in situ hybridization to polytene chromosomes of ovarian nurse cells of the mosquito Anopheles gambiae. As part of this effort, we have developed a vigorous pink-eyed laboratory strain of A. gambiae (PEST), rendered homozygous standard for chromosomal inversions on all autosomes. Ten different individuals of this strain were studied with each transposable element probe. The average number of hybridization sites per genome was 83.9 for T1, 63.4 for Q, 31.5 for Pegasus and 64.7 for mariner, excluding pericentric and centromeric regions. However, some degree of polymorphism was observed within each family such that, considering all ten individuals, 94 different sites were detected for T1, 82 sites for Q, 45 sites for Pegasus and 71 sites for mariner. The mean occupancy per site varied from 0.70 (Pegasus) to 0.91 (mariner), which, while significantly higher than that seen for transposable elements in natural populations of Drosophila melanogaster, is comparable to that seen in established laboratory stocks. In addition, these element families were not randomly distributed. All but Pegasus were concentrated in centromeric heterochromatin and centromere-proximal euchromatin, most showed a deficit of hybridization sites in the distal section of chromosomes, and a significant proportion of sites were coincident between families. These results provide the first detailed examination of the cytogenetic location of transposable elements in a nondrosophilid insect, and, through comparison with the behavior of transposable elements in Drosophila, may provide insight into the interaction between elements and host. The mapped elements are also expected to serve as landmarks useful in integrating the developing     

Comparative analysis of Stowaway-like miniature inverted repeat transposable elements in wheat group 7 chromosomes: Abundance,composition, and evolution

Miniature inverted repeat transposable elements (MITEs) are the most ubiquitous transposable elements in eukaryotic genomes; they play a prominent role in sequence divergence and genome evolution. There are many well-characterized Stowaway-like MITE families in wheat, but their distribution, abundance, and composition at the chromosome level are still not well understood. In this study, we systematically investigated the Stowaway-like MITEs in wheat group 7 chromosomes based on the survey sequences of isolated wheat chromosomes, to compare them at the chromosome level and to reveal their evolutionary role on wheat polyploidization. In summary, 2026 MITEs were identified, of which 587, 714, and 725 were distributed on 7A, 7B, and 7D chromosomes, respectively. There are more MITEs present on 7D, compared to 7A and 7B, suggesting A and B subgenomes eliminated some repetitive elements during two hybridization processes. Furthermore, some chromosome/arm-specific MITEs were also identified, providing information on the function and evolution of MITEs in wheat genomes. The sequence diversity of the MITE insertions was also investigated. This study for the first time investigated the abundance and composition of MITEs at the chromosome level, which will be beneficial to improve our understanding of the distribution of wheat MITEs and their evolutionary role in polyploidization.     

Microsatellites, transposable elements and the X chromosome

Variability at microsatellite (MS) loci is generally perceived as resulting from an interaction between mutation and genetic drift and, to a lesser extent, selection and recombination. Less investigated has been the reason for MS accumulation in genomes. We present here a simple model that could account for the variation in density of MS loci, assuming that they are created either through replication slippage or in association with transposable elements. Microsatellites then evolve under the forces cited above. We use this framework to revisit two results obtained from high-density genomic maps of the human and mouse genomes built with thousands of CA repeats: MS loci are (1) less variable and (2) less dense on the X chromosome than on autosomes. The first result is most likely explained by differential mutation on the X chromosome and the autosomes. The second result may be explained by differential mutation, provided the distributions of MS loci are still not at equilibrium. Selection, acting either directly on large allele size or indirectly on the transposable elements associated with MS, may explain the same result. The framework developed here is a first step toward more rigorous models, calling for additional data.      

Transposable elements in individual genotypes of Drosophila simulans

Transposable elements are abundant, dynamic components of the genome that affect organismal phenotypes and fitness. In Drosophila melanogaster, they have increased in abundance as the species spread out of Africa, and different populations differ in their transposable element content. However, very little is currently known about how transposable elements differ between individual genotypes, and how that relates to the population dynamics of transposable elements overall. The sister species of D. melanogaster, D. simulans, has also recently become cosmopolitan, and panels of inbred genotypes exist from cosmopolitan and African flies. Therefore, we can determine whether the differences in colonizing populations are repeated in D. simulans, what the dynamics of transposable elements are in individual genotypes, and how that compares to wild flies. After estimating copy number in cosmopolitan and African D. simulans, I find that transposable element load is higher in flies from cosmopolitan populations. In addition, transposable element load varies considerably between populations, between genotypes, but not overall between wild and inbred lines. Certain genotypes either contain active transposable elements or are more permissive of transposition and accumulate copies of particular transposable elements. Overall, it is important to quantify genotype‐specific transposable element dynamics as well as population averages to understand the dynamics of transposable element accumulation over time.     

Frequent transpositions of Drosophila melanogaster HeT-A transposable elements to receding chromosome ends.

HeT-A elements are a new family of transposable elements in Drosophila that are found exclusively in telomeric regions and in the pericentric heterochromatin. Transposition of these elements onto broken chromosome ends has been implicated in chromosome healing. To monitor the fate of HeT-A elements that had attached to broken ends of the X chromosome, we examined individual X chromosomes from a defined population over a period of 17 generations. The ends of the X chromosomes with new HeT-A additions receded at the same rate as the broken ends before the HeT-A elements attached. In addition, some chromosomes, approximately 1% per generation, had acquired new HeT-A sequences of an average of 6 kb at their ends with oligo(A) tails at the junctions. Thus, the rate of addition of new material per generation matches the observed rate of terminal loss (70-75 bp) caused by incomplete replication at the end of the DNA molecule. One such recently transposed HeT-A element which is at least 12 kb in length has been examined in detail. It contains a single open reading frame of 2.8 kb which codes for a gag-like protein.     

Transposable elements and fitness in Drosophila melanogaster

Transposable elements constitute a significant fraction of the Drosophila melanogaster genome. The five families of moderately repeated transposable elements identified to date occupy dispersed and variable genomic locations, but have relatively constant copy numbers per individual. What effect to these elements have on the fitness of the individuals harboring them? Experimental evidence relating to this question is reviewed. The relevant data fall into two broad categories. The first involves the determination of the distribution of transposable elements in natural populations, by restriction mapping or in situ hybridization, and the comparison of the observed distribution with different theoretical expectations. The second approach is to study directly the effects of new transposable element-induced mutations on fitness. The P family of transposable elements is a particularly efficient mutagen, and the results of experiments in which initially P-free chromosomes are contaminated with P elements are discussed with regard to P-induced fitness mutations.     

Population genetics of transposable DNA elements

This paper is an attempt to bring together the various, dispersed data published in the literature on insertion polymorphism of transposable elements from various kinds of populations (natural populations, laboratory strains, isofemale and inbred lines). Although the results deal mainly with Drosophila, data on other organisms have been incorporated when necessary to illustrate the discussion. The data pertinent to the regions of insertion, the rates of transposition and excision, the copy number regulation, and the degree of heterozygosity were analysed in order to be confronted with the speculations made with various theoretical models of population biology of transposable elements. The parameters of these models are very sensitive to the values of the transposable element characteristics estimated on populations, and according to the difficulties of these estimations (population not at equilibrium, particular mutations used to estimate the transposition and excision rates, trouble with the in situ technique used to localize the insertions, undesired mobilization of TEs in crosses, spontaneous genome resetting, environmental effects, etc.) it cannot be decided accurately which model better accounts for the population dynamics of these TEs. Tendencies, however, emerge in Drosophila: the copia element shows evidence for deficiency of insertions on the X chromosomes, a result consistent with selection against mutational effects of copia insertions; the P element repartition does not significantly deviate from the neutral assumption, in spite of a systematic copy number of insertions higher on the X than on the autosomes. Data on other elements support either the neutral model of TE containment, neither of the two models, or both. Prudence in conclusion should then be de rigueur when dealing with such kind of data. Finally the potential roles of TEs in population adaptation and evalution are discussed.     

The transposable elements of the Drosophila melanogaster euchromatin: a genomics perspective

Background

Transposable elements are found in the genomes of nearly all eukaryotes. The recent completion of the Release 3 euchromatic genomic sequence of Drosophila melanogaster by the Berkeley Drosophila Genome Project has provided precise sequence for the repetitive elements in the Drosophila euchromatin. We have used this genomic sequence to describe the euchromatic transposable elements in the sequenced strain of this species.

Results

We identified 85 known and eight novel families of transposable element varying in copy number from one to 146. A total of 1,572 full and partial transposable elements were identified, comprising 3.86% of the sequence. More than two-thirds of the transposable elements are partial. The density of transposable elements increases an average of 4.7 times in the centromere-proximal regions of each of the major chromosome arms. We found that transposable elements are preferentially found outside genes; only 436 of 1,572 transposable elements are contained within the 61.4 Mb of sequence that is annotated as being transcribed. A large proportion of transposable elements is found nested within other elements of the same or different classes. Lastly, an analysis of structural variation from different families reveals distinct patterns of deletion for elements belonging to different classes.

Conclusions

This analysis represents an initial characterization of the transposable elements in the Release 3 euchromatic genomic sequence of D. melanogaster for which comparison to the transposable elements of other organisms can begin to be made. These data have been made available on the Berkeley Drosophila Genome Project website for future analyses.     

Genome-wide comparison of cyanobacterial transposable elements, potential genetic diversity indicators

Transposable elements are widely distributed in archaea, bacteria and eukarya domains. Considerable discrepancies of transposable elements in eukaryotes have been reported, however, the studies focusing on the diversity of transposable element systems in prokaryotes were scarce. Understanding the transposable element system in cyanobacteria by the genome-wide analysis will greatly improve the knowledge of cyanobacterial diversity. In this study, the transposable elements of seventeen cyanobacterial genomes were analyzed. The abundance of insertion sequence (IS) elements differs significantly among the cyanobacterial genomes examined. In particular, water bloom forming Microcystis aeruginosa NIES843 was shown to have the highest abundance of IS elements reaching 10.85% of the genome. IS family is a widely acceptable IS classification unit, and IS subfamily, based on probe sequences, was firstly proposed as the basic classification unit for IS element system, therefore both IS family and IS subfamily were suggested as the two hierarchical units for evaluating the IS element system diversity. In total, 1980 predicted IS elements, within 21 IS families and 132 subfamilies, were identified in the examined cyanobacterial genomes. Families IS4, IS5, IS630 and IS200-605 are widely distributed, and therefore supposed to be the ancestral IS families. Analysis on the intactness of IS elements showed that the percentage of the intact IS differs largely among these cyanobacterial strains. Higher percentage of the intact IS detected in the two hot spring cyanobacterial strains implied that the intactness of IS elements may be related to the genomic stabilization of cyanobacteria inhabiting in the extreme environments. The frequencies between IS elements and miniature inverted-repeat transposable elements (MITEs) were shown to have a linear positive correlation. The transposable element system in cyanobacterial genomes is of hypervariability. With characterization of easy definition and stability, IS subfamily is considered as a reliable lower classification unit in IS element system. The abundance of intact IS, the composition of IS families and subfamilies, the sequence diversity of IS element nucleotide and transposase amino acid are informative and suitable as the indicators for studies on cyanobacterial diversity. Practically, the transposable system may provide us a new perspective to realize the diversity and evolution of populations of water bloom forming cyanobacterial species.     

Intragenomic distribution and stability of transposable elements in euchromatin and heterochromatin of drosophila melanogaster: non-LTR retrotransposon

The intragenomic location of the elements of the I, G, jockey, F, and Doc transposon families has been studied by the Southern blot analysis, in 12 laboratory Drosophila melanogaster stocks. Elements located in euchromatin, heterochromatin, and on the Y chromosome are identified, and their stability has been assessed by comparing the autoradiographs detected in different stocks and analysis of individual flies. Evidence is shown suggesting that preferential location in euchromatin or heterochromatin and the distribution within heterochromatin are distinctive of transposon families. Elements located in heterochromatin can be unstable. These results are discussed in the context of the relationship between transposable elements and the host genome. Received: 21 August 1996 / Accepted: 24 March 1997     

Inferring the history of interchromosomal gene transposition in Drosophila using n-dimensional parsimony

Gene transposition puts a new gene copy in a novel genomic environment. Moreover, genes moving between the autosomes and the X chromosome experience change in several evolutionary parameters. Previous studies of gene transposition have not utilized the phylogenetic framework that becomes possible with the availability of whole genomes from multiple species. Here we used parsimonious reconstruction on the genomic distribution of gene families to analyze interchromosomal gene transposition in Drosophila. We identified 782 genes that have moved chromosomes within the phylogeny of 10 Drosophila species, including 87 gene families with multiple independent movements on different branches of the phylogeny. Using this large catalog of transposed genes, we detected accelerated sequence evolution in duplicated genes that transposed when compared to the parental copy at the original locus. We also observed a more refined picture of the biased movement of genes from the X chromosome to the autosomes. The bias of X-to-autosome movement was significantly stronger for RNA-based movements than for DNA-based movements, and among DNA-based movements there was an excess of genes moving onto the X chromosome as well. Genes involved in female-specific functions moved onto the X chromosome while genes with male-specific functions moved off the X. There was a significant overrepresentation of proteins involving chromosomal function among transposed genes, suggesting that genetic conflict between sexes and among chromosomes may be a driving force behind gene transposition in Drosophila.