Tempo and mode of Ty element evolution in Saccharomyces cerevisiae

The Saccharomyces cerevisiae genome contains five families of long terminal repeat (LTR) retrotransposons, Ty1-Ty5. The sequencing of the S. cerevisiae genome provides an unprecedented opportunity to examine the patterns of molecular variation existing among the entire genomic complement of Ty retrotransposons. We report the results of an analysis of the nucleotide and amino acid sequence variation within and between the five Ty element families of the S. cerevisiae genome. Our results indicate that individual Ty element families tend to be highly homogenous in both sequence and size variation. Comparisons of within-element 5' and 3' LTR sequences indicate that the vast majority of Ty elements have recently transposed. Furthermore, intrafamily Ty sequence comparisons reveal the action of negative selection on Ty element coding sequences. These results taken together suggest that there is a high level of genomic turnover of S. cerevisiae Ty elements, which is presumably in response to selective pressure to escape host-mediated repression and elimination mechanisms.     

Genomic demography: a life-history analysis of transposable element evolution.

Retrotransposons are ubiquitous mobile genetic elements that have played a significant role in shaping eukaryotic genome evolution. The genome of the yeast Saccharomyces cerevisiae harbours five families of retrotransposons, Ty1-Ty5. With the publication of the S. cerevisiae genome sequence, for the first time a full genomic complement of retrotransposon sequences is available. Analysis of these sequences promises to yield insight into the nature of host--transposon coevolution. Evolutionary change in Ty elements depends on their replication and excision rates, which have been determined in the laboratory. Rates measured in the laboratory may differ from those that have operated over evolutionary time. Based on an analysis of sequence data for the Ty1, Ty2 and hybrid Ty1/2 families, we develop a novel 'genomic demography' model to estimate long-term transposition and excision rates and to estimate how long ago these elements entered the yeast genome. We find that rates of excision and transposition have averaged 7.2-8.7 x 10(-8) per generation over evolutionary time. Two separate models provide upper- and lower-bound estimates for the age of the system, suggesting that the first elements entered the genome between approximately 50 million and 250 million generations ago.     

Evidence for the Role of Recombination in the Regulatory Evolution of Saccharomyces cerevisiae Ty Elements

The recent completion of the sequencing of the Saccharomyces cerevisiae genome provides a unique opportunity to analyze the evolutionary relationships existing among the entire complement of retrotransposons residing within a single genome. In this article we report the results of such an analysis of two closely related families of yeast long terminal repeat (LTR) retrotransposons, Ty1 and Ty2. In our study, we analyzed the molecular variation existing among the 32 Ty1 and 13 Ty2 elements present within the S. cerevisiae genome recently sequenced within the context of the yeast genome project. Our results indicate that while the Ty1 family is most likely ancestral to Ty2 elements, both families of elements are relatively recent components of the S. cerevisiae genome. Our results also indicate that both families of elements have been subject to purifying selection within their protein coding regions. Finally, and perhaps most interestingly, our results indicate that a relatively recent recombination event has occurred between Ty2 and a subclass of Ty1 elements involving the LTR regulatory region. We discuss the possible biological significance of these findings and, in particular, how they contribute to a better overall understanding of LTR retrotransposon evolution. Received: 30 September 1997 / Accepted: 3 February 1998     

The Role of Interelement Selection in Saccharomyces cerevisiae Ty Element Evolution

Retrotransposons are mobile genetic elements that are ubiquitous components of eukaryotic genomes. The evolutionary success of retrotransposons is explained by their ability to replicate faster than the host genomes in which they reside. Elements with higher rates of genomic replication possess a selective advantage over less active elements. Retrotransposon populations, therefore, are shaped largely by selective forces acting at the genomic level between elements. To evaluate rigorously the effects of selective forces acting on retrotransposons, detailed information on the patterns of molecular variation within and between retrotransposon families is needed. The sequencing of the Saccharomyces cerevisiae genome, which includes the entire genomic complement of yeast retrotransposons, provides an unprecedented opportunity to access and analyze such data. In this study, we analyzed in detail the patterns of nucleotide variation within the open reading frames of two parental (Ty1 and Ty2) and one hybrid (Ty1/2) family of yeast retrotransposons. The pattern and distribution of nucleotide changes on the phylogenetic reconstructions of the three families of Ty elements reveal evidence of negative selection on both internal and external branches of the Ty phylogenies. These results indicate that most, if not all, Ty elements examined represent active or recently active retrotransposon lineages. We discuss the relevance of these findings with respect to the coevolutionary dynamic operating between genomic element populations and the host organisms in which they reside. Received: 5 November 1998 / Accepted: 17 March 1999     

Evolutionary Genomics of Transposable Elements in Saccharomyces cerevisiae

Saccharomyces cerevisiae is one of the premier model systems for studying the genomics and evolution of transposable elements. The availability of the S. cerevisiae genome led to unprecedented insights into its five known transposable element families (the LTR retrotransposons Ty1-Ty5) in the years shortly after its completion. However, subsequent advances in bioinformatics tools for analysing transposable elements and the recent availability of genome sequences for multiple strains and species of yeast motivates new investigations into Ty evolution in S. cerevisiae. Here we provide a comprehensive phylogenetic and population genetic analysis of all Ty families in S. cerevisiae based on a systematic re-annotation of Ty elements in the S288c reference genome. We show that previous annotation efforts have underestimated the total copy number of Ty elements for all known families. In addition, we identify a new family of Ty3-like elements related to the S. paradoxus Ty3p which is composed entirely of degenerate solo LTRs. Phylogenetic analyses of LTR sequences identified three families with short-branch, recently active clades nested among long branch, inactive insertions (Ty1, Ty3, Ty4), one family with essentially all recently active elements (Ty2) and two families with only inactive elements (Ty3p and Ty5). Population genomic data from 38 additional strains of S. cerevisiae show that the majority of Ty insertions in the S288c reference genome are fixed in the species, with insertions in active clades being predominantly polymorphic and insertions in inactive clades being predominantly fixed. Finally, we use comparative genomic data to provide evidence that the Ty2 and Ty3p families have arisen in the S. cerevisiae genome by horizontal transfer. Our results demonstrate that the genome of a single individual contains important information about the state of TE population dynamics within a species and suggest that horizontal transfer may play an important role in shaping the genomic diversity of transposable elements in unicellular eukaryotes.     

Increased Length of Long Terminal Repeats Inhibits Ty1 Transposition and Leads to the Formation of Tandem Multimers

The Ty1 retrotransposon of Saccharomyces cerevisiae is bounded by long-terminal repeats (LTRs). We have constructed a variety of Ty1 elements in which the LTR length has been increased from the normal length of 334 bp to >2 kb. Although small insertions in the LTR have minimal effects on transposition frequency, larger insertions dramatically reduce it. Nevertheless, elements with long LTRs are incorporated into the genome at a low frequency. Most of these rare insertion events represent Ty1 tandem (head to tail) multimers.     

Structural and evolutionary analyses of the Ty3/gypsy group of LTR retrotransposons in the genome of Anopheles gambiae

The recent availability of the genome of Anopheles gambiae offers an extraordinary opportunity for comparative studies of the diversity of transposable elements (TEs) and their evolutionary dynamics between two related species, taking advantage of the existing information from Drosophila melanogaster. To this goal, we screened the genome of A. gambiae for elements belonging to the Ty3/gypsy group of long-terminal repeat (LTR) retrotransposons. The A. gambiae genome displays a rich diversity of LTR retrotransposons, clearly greater than D. melanogaster. We have characterized in detail 63 families, belonging to five of the nine main lineages of the Ty3/gypsy group. The Mag lineage is the most diverse and abundant, with more than 30 families. In sharp contrast with this finding, a single family belonging to this lineage has been found in D. melanogaster, here reported for the first time in the literature, most probably consisting of old inactive elements. The CsRn1 lineage is also abundant in A. gambiae but almost absent from D. melanogaster. Conversely, the Osvaldo lineage has been detected in Drosophila but not in Anopheles. Comparison of structural characteristics of different families led to the identification of several lineage-specific features such as the primer-binding site (PBS), the gag-pol translational recoding signal (TRS), which is extraordinarily diverse within the Ty3/gypsy retrotransposons of A. gambiae, or the presence/absence of specific amino acid motifs. Interestingly, some of these characteristics, although in general well conserved within lineages, may have evolved independently in particular branches of the phylogenetic tree. We also show evidence of recent activity for around 75% of the families. Nevertheless, almost all families contain a high proportion of degenerate members and solitary LTRs (solo LTRs), indicative of a lower turnover rate of retrotransposons belonging to the Ty3/gypsy group in A. gambiae than in D. melanogaster. Finally, we have detected significant overrepresentations of insertions on the X chromosome versus autosomes and of putatively active insertions on euchromatin versus heterochromatin.     

A computational study of the dynamics of LTR retrotransposons in the Populus trichocarpa genome

Retrotransposons are an ubiquitous component of plant genomes, especially abundant in species with large genomes. Populus trichocarpa has a relatively small genome, which was entirely sequenced; however, studies focused on poplar retrotransposons dynamics are rare. With the aim to study the retrotransposon component of the poplar genome, we have scanned the complete genome sequence searching full-length long-terminal repeat (LTR) retrotransposons, i.e., characterised by two long terminal repeats at the 5′ and 3′ ends. A computational approach based on detection of conserved structural features, on building multiple alignments, and on similarity searches was used to identify 1,479 putative full-length LTR retrotransposons. Ty1-copia elements were more numerous than Ty3-gypsy. However, many LTR retroelements were not assigned to any superfamily because lacking of diagnostic features and non-autonomous. LTR retrotransposon remnants were by far more numerous than full-length elements, indicating that during the evolution of poplar, large amplification of these elements was followed by DNA loss. Within superfamilies, Ty3-gypsy families are made of more members than Ty1-copia ones. Retrotransposition occurred with increasing frequency following the separation of Populus sections, with different waves of retrotransposition activity between Ty3-gypsy and Ty1-copia elements. Recently inserted elements appear more frequently expressed than older ones. Finally, different levels of activity of retrotransposons were observed according to their position and their density in the linkage groups. On the whole, the results support the view of retrotransposons as a community of different organisms in the genome, whose activity (both retrotransposition and DNA loss) has heavily impacted and probably continues to impact poplar genome structure and size.     

Retrotransposon insertion polymorphisms in six rice genes and their evolutionary history

Retrotransposons are abundant in higher plant genomes. Although retrotransposons associated with plant genes have been identified, little is known about their evolutionary conservation at the level of species and subspecies. In the present study, we investigated the phylogenetic distribution of long terminal repeat (LTR) retrotransposon, long interspersed nuclear element (LINE) and short interspersed nuclear element (SINE) insertions in six genes in 95 cultivated and wild rice genotypes. These six genes are likely to be functional based on nonsynonymous (Ka) to synonymous (Ks) substitution ratios which were found to be significantly <1. Different conservation patterns of these retrotransposons in genes were observed in cultivated and wild rice species. Four out of seven retrotransposon insertions appear to predate the ancestral Oryza AA genome. Two of these insertions in genes 4 and 5 occurred early in the evolutionary history of Oryza. Two retrotransposon insertions in gene 1 arose after the divergence of Asian cultivated rice from its wild ancestor. Furthermore, the retrotransposon insertion in gene 3 appears to have occurred in the ancestral lineage leading to temperate japonicas. Conservation of retrotransposon insertions in genes in specific groups, species, and lineages might be related to their specific function.     

Survey of long terminal repeat retrotransposons of domesticated silkworm (Bombyx mori)

Long terminal retrotransposons are major components of eukaryotic transposable elements. We have surveyed the long terminal repeats (LTR) retrotransposons of domesticated silkworm (Bombyx mori) by mining the data produced by Bombyx mori Genome Sequencing Project. At least 29 separate families of LTR retrotransposons are identified in this survey, comprising of 11.8% of the complete sequence. Families of domesticated silkworm LTR retrotransposons can be mainly classified into three groups: gypsy-like, copia-like, Pao-Bel. Fourteen families identified consist of gypsy-like elements, four families consist of copia-like elements and seven families consist of Pao-Bel elements. In addition to the three groups of LTR retrotransposons, two families of unusual non-coding elements are identified in the genome of this species. Further phylogenetic analysis of RT domain indicates that the elements of B.mori show high diversity and can form different clades in each group. An analysis of sequence variation from different families reveals distinct patterns of variation for the elements belonging to three groups. The analysis of the domesticated silkworm LTR retrotransposons should assist in our understanding of the roles of retroelement in lepidopteron insect genome evolution.     

Identification of novel LTR retrotransposons in the genome of Aedes aegypti

We have detected seventy-six novel LTR retrotransposons in the genome of the mosquito Aedes aegypti by a genome wide analysis using the LTR_STRUC program. We have performed a phylogenetic classification of these novel elements and a distribution analysis in the genome of A. aegypti. These mobile elements belong either to the Ty3/gypsy or to the Bel family of retrotransposons and were not annotated in the mosquito LTR retrotransposon database (TEfam). We have found that  1.8% of the genome is occupied by these newly detected retrotransposons that are distributed predominantly in intergenic genomic sequences and introns. The potential role of retrotransposon insertions linked to host genes is described and discussed. We show that a retrotransposon family belonging to the Osvaldo lineage has peculiar structural features, and its presence is likely to be restricted to the A. aegypti and to the Culex pipiens quinquefasciatus genomes. Furthermore we show that the ninja-like group of elements lacks the Primer Binding Site (PBS) sequence necessary for the replication of retrotransposons. These results integrate the knowledge on the complicate genomic structure of an important disease vector.     

Fitness Effects of Ty Transposition in Saccharomyces Cerevisiae

It has been suggested that the primary evolutionary role of transposable elements is negative and parasitic. Alternatively, the target specificity and gene regulatory capabilities of many transposable elements raise the possibility that transposable element-induced mutations are more likely to be adaptively favorable than other types of mutations. Populations of Saccharomyces cerevisiae containing large amounts of variation for Ty1 genomic insertions were constructed, and the effects of Ty1 copy number on two components of fitness, yield and growth rate were determined. Although mean stationary phase density decreased with increased Ty1 copy number, the variance and range increased. The distributions of stationary phase densities indicate that many Ty1 insertions have negative effects on fitness, but also that some may have positive effects. To test directly for adaptively favorable Ty1 insertions, populations containing large amounts of variability for Ty1 copy number were grown in continuous culture. After 98-112 generations the frequency of clones containing zero Ty1 elements had decreased to approximately 0.0, and specific Ty1-containing clone families had predominated. Considering that most of the genetic variation in the populations was due to Ty1 transposition, and that Ty1 insertions had, on average, a negative effect on fitness, we conclude that Ty1 transposition events were directly responsible for the production of adaptive mutations in the clones that predominated in the populations.     

家蚕LTR逆转录转座子的鉴定、分类及系统发育分析

转座子是真核生物基因组的重要组成成分。为了研究家蚕Bombyx mori长末端重复序列 (long terminal repeat, LTR)逆转录转座子的分类及进化, 本研究采用de novo预测和同源性搜索相结合的方法, 在家蚕基因组中共鉴定出了38个LTR逆转录转座子家族, 序列长度占整个基因组的0.64%, 远小于先前预测的11.8%, 其中有6个家族为本研究的新发现。38个家族中, 26个家族有表达序列标签 (expression sequence tag, EST)证据, 表明这些家族具有潜在的活性。对有EST证据的6个家族和没有EST证据的5个家族用RT-PCR进行了组织表达谱实验, 结果表明这11个家族在一些组织中有表达, 这进一步证实了这些家族具有转录活性, 基于此我们推测家蚕中大部分的LTR逆转录转座子家族很可能具有潜在活性。对转座子的插入时间进行估计, 结果表明绝大部分元件都是最近1百万年内插入到家蚕基因组中的。我们还比较了黑腹果蝇Drosophila melanogaster、 冈比亚按蚊Anopheles gambiae和家蚕B. mori中Ty3/Gypsy超家族分支的差异, 结果表明不同枝在不同昆虫中有着不同的扩张。家蚕中LTR逆转录转座子的鉴定和系统分析有助于我们理解逆转录转座子在昆虫进化中的作用。     

Genome evolution mediated by Ty elements in Saccharomyces

How mobile genetic elements molded eukaryotic genomes is a key evolutionary question that gained wider popularity when mobile DNA sequences were shown to comprise about half of the human genome. Although Saccharomyces cerevisiae does not suffer such "genome obesity", five families of LTR-retrotransposons, Ty1, Ty2, Ty3, Ty4, and Ty5 elements, comprise about 3% of its genome. The availability of complete genome sequences from several Saccharomyces species, including members of the closely related sensu stricto group, present new opportunities for analyzing molecular mechanisms for chromosome evolution, speciation, and reproductive isolation. In this review I present key experiments from both the pre- and current genomic sequencing eras suggesting how Ty elements mediate genome evolution.     

The Saccharomyces retrotransposon Ty5 influences the organization of chromosome ends.

Retrotransposons are ubiquitous components of eukaryotic genomes suggesting that they have played a significant role in genome organization. In Saccharomyces cerevisiae, eight of 10 endogenous insertions of the Ty5 retrotransposon family are located within 15 kb of chromosome ends, and two are located near the subtelomeric HMR locus. This genomic organization is the consequence of targeted transposition, as 14 of 15 newly transposed Ty5 elements map to telomeric regions on 10 different chromosomes. Nine of these insertions are within 0.8 kb and three are within 1.5 kb of the autonomously replicating consensus sequence in the subtelomeric X repeat. This suggests that the X repeat plays an important role in directing Ty5 integration. Analysis of endogenous insertions from S.cerevisiae and its close relative S.paradoxus revealed that only one of 12 insertions has target site duplications, indicating that recombination occurs between elements. This is further supported by the observation that Ty5 insertions mark boundaries of sequence duplications and rearrangements in these species. These data suggest that transposable elements like Ty5 can shape the organization of chromosome ends through both transposition and recombination.