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     

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.     

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。     

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.     

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.     

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.     

酵母Ty1和Ty3转座调控机制研究进展

LTR(Long Terminal Repetition, LTR)反转录转座子广泛存在于真核生物界,是逆转录病毒的进化祖先。LTR反转录转座子有两个古老的家族,Ty1/Copia和Ty3/Gypsy。目前关于LTR反转录转座子转座机制及调控机制研究最透彻的是来源于酵母的两个活性转座子Ty1和Ty3。全面综述了Ty1和Ty3的分子生物学机制相关的最新研究进展。系统总结了Ty1和Ty3的结构特征及转座特性,归纳了Ty1和Ty3与宿主共生的调控机制,为进一步了解酵母LTR反转录转座子相关转座调控机制提供参考。     

Proliferation of Ty3/gypsy-like retrotransposons in hybrid sunflower taxa inferred from phylogenetic data

Background  

Long terminal repeat (LTR) retrotransposons are a class of mobile genetic element capable of autonomous transposition via an RNA intermediate. Their large size and proliferative ability make them important contributors to genome size evolution, especially in plants, where they can reach exceptionally high copy numbers and contribute substantially to variation in genome size even among closely related taxa. Using a phylogenetic approach, we characterize dynamics of proliferation events of Ty3/gypsy-like LTR retrotransposons that led to massive genomic expansion in three Helianthus (sunflower) species of ancient hybrid origin. The three hybrid species are independently derived from the same two parental species, offering a unique opportunity to explore patterns of retrotransposon proliferation in light of reticulate evolutionary events in this species group.     

Network dynamics of eukaryotic LTR retroelements beyond phylogenetic trees

Background  

Sequencing projects have allowed diverse retroviruses and LTR retrotransposons from different eukaryotic organisms to be characterized. It is known that retroviruses and other retro-transcribing viruses evolve from LTR retrotransposons and that this whole system clusters into five families: Ty3/Gypsy, Retroviridae, Ty1/Copia, Bel/Pao and Caulimoviridae. Phylogenetic analyses usually show that these split into multiple distinct lineages but what is yet to be understood is how deep evolution occurred in this system.     

Diversity of LTR-retrotransposons and <Emphasis Type="Italic">Enhancer/Suppressor</Emphasis><Emphasis Type="Italic">Mutator</Emphasis>-like transposons in cassava (<Emphasis Type="Italic">Manihot esculenta</Emphasis> Crantz)

Cassava (Manihot esculenta Crantz), though a major world crop with enormous potential, is very under studied. Little is known about its genome structure and organisation. Transposable elements have a key role in the evolution of genome structure, and can be used as important tools in applied genetics. This paper sets out to survey the diversity of members of three major classes of transposable element within the cassava genome and in relation to similar elements in other plants. Members of two classes of LTR-retrotransposons, Ty1/copia-like and Ty3/gypsy-like, and of Enhancer/Suppressor Mutator (En/Spm)-like transposons were isolated and characterised. Analyses revealed 59 families of Ty1/copia, 26 families of Ty3/gypsy retrotransposons, and 40 families of En/Spm in the cassava genome. In the comparative analyses, the predicted amino acid sequences for these transposon classes were compared with those of related elements from other plant species. These revealed that there were multiple lineages of Ty1/copia-like retrotransposons in the genome of cassava and suggested that vertical and horizontal transmission as the source of cassava Mecops may not be mutually exclusive. For the Ty3/gypsy elements network, two groups of cassava Megyps were evident including the Arabidopsis Athila lineage. However, cassava En/Spm-like elements (Meens) constituted a single group within a network of plant En/Spm-like elements. Hybridisation analysis supported the presence of transposons in the genome of cassava in medium (Ty3/gypsy and En/Spm) to high (Ty1/copia) copy numbers. Thus the cassava genome was shown to contain diverse members of three major classes of transposable element; however, the different classes exhibited contrasting evolutionary histories.     

Mosquitoes LTR retrotransposons: a deeper view into the genomic sequence of Culex quinquefasciatus

A set of 67 novel LTR-retrotransposon has been identified by in silico analyses of the Culex quinquefasciatus genome using the LTR_STRUC program. The phylogenetic analysis shows that 29 novel and putatively functional LTR-retrotransposons detected belong to the Ty3/gypsy group. Our results demonstrate that, by considering only families containing potentially autonomous LTR-retrotransposons, they account for about 1% of the genome of C. quinquefasciatus. In previous studies it has been estimated that 29% of the genome of C. quinquefasciatus is occupied by mobile genetic elements.The potential role of retrotransposon insertions strictly associated with host genes is described and discussed along with the possible origin of a retrotransposon with peculiar Primer Binding Site region. Finally, we report the presence of a group of 38 retrotransposons, carrying tandem repeated sequences but lacking coding potential, and apparently lacking "master copy" elements from which they could have originated. The features of the repetitive sequences found in these non-autonomous LTR retrotransposons are described, and their possible role discussed.These results integrate the existing data on the genomics of an important virus-borne disease vector.     

Major repeat components covering one‐third of the ginseng (Panax ginseng C.A. Meyer) genome and evidence for allotetraploidy

Ginseng (Panax ginseng) is a famous medicinal herb, but the composition and structure of its genome are largely unknown. Here we characterized the major repeat components and inspected their distribution in the ginseng genome. By analyzing three repeat‐rich bacterial artificial chromosome (BAC) sequences from ginseng, we identified complex insertion patterns of 34 long terminal repeat retrotransposons (LTR‐RTs) and 11 LTR‐RT derivatives accounting for more than 80% of the BAC sequences. The LTR‐RTs were classified into three Ty3/gypsy (PgDel, PgTat and PgAthila) and two Ty1/Copia (PgTork and PgOryco) families. Mapping of 30‐Gbp Illumina whole‐genome shotgun reads to the BAC sequences revealed that these five LTR‐RT families occupy at least 34% of the ginseng genome. The Ty3/Gypsy families were predominant, comprising 74 and 33% of the BAC sequences and the genome, respectively. In particular, the PgDel family accounted for 29% of the genome and presumably played major roles in enlargement of the size of the ginseng genome. Fluorescence in situ hybridization (FISH) revealed that the PgDel1 elements are distributed throughout the chromosomes along dispersed heterochromatic regions except for ribosomal DNA blocks. The intensity of the PgDel2 FISH signals was biased toward 24 out of 48 chromosomes. Unique gene probes showed two pairs of signals with different locations, one pair in subtelomeric regions on PgDel2‐rich chromosomes and the other in interstitial regions on PgDel2‐poor chromosomes, demonstrating allotetraploidy in ginseng. Our findings promote understanding of the evolution of the ginseng genome and of that of related species in the Araliaceae.