PIF- and Pong-like transposable elements: distribution, evolution and relationship with Tourist-like miniature inverted-repeat transposable elements

Miniature inverted-repeat transposable elements (MITEs) are short, nonautonomous DNA elements that are widespread and abundant in plant genomes. Most of the hundreds of thousands of MITEs identified to date have been divided into two major groups on the basis of shared structural and sequence characteristics: Tourist-like and Stowaway-like. Since MITEs have no coding capacity, they must rely on transposases encoded by other elements. Two active transposons, the maize P Instability Factor (PIF) and the rice Pong element, have recently been implicated as sources of transposase for Tourist-like MITEs. Here we report that PIF- and Pong-like elements are widespread, diverse, and abundant in eukaryotes with hundreds of element-associated transposases found in a variety of plant, animal, and fungal genomes. The availability of virtually the entire rice genome sequence facilitated the identification of all the PIF/Pong-like elements in this organism and permitted a comprehensive analysis of their relationship with Tourist-like MITEs. Taken together, our results indicate that PIF and Pong are founding members of a large eukaryotic transposon superfamily and that members of this superfamily are responsible for the origin and amplification of Tourist-like MITEs.     

昆虫的转座子及其功能

转座子是一类散布在基因组中序列重复的DNA片段,它们可以通过特定转座酶在基因组中移动.目前测序的真核生物基因组的结果都显示转座子占基因组中相当大的一部分.目前对于转座子功能的研究主要集中在产生新功能、修饰染色质、保护生殖细胞,以及参与基因组的协同进化上.随着对其功能研究的深入,利用转座子转座能力开发的转基因系统可以改造物种的遗传性状.此外转座子还可以作为一个标尺用以分析物种进化关系.     

First evidence of miniature transposable elements in sponges (Porifera)

Transposable elements play a vital role in genome evolution and may have been important for the formation of the early metazoan genome, but only little is known about transposons at this interface between unicellular opisthokonts and Metazoa. Here, we describe the first miniature transposable elements (MITEs, Queen1 and Queen2) in sponges. Queen1 and Queen2 are probably derived from Tc1/mariner-like MITE families and are represented in more than 3,800 and 1,700 copies, respectively, in the Amphimedon queenslandica genome. Queen elements are located in intergenic regions as well as in introns, providing the potential to induce new splicing sites and termination signals in the genes. Further possible impacts of MITEs on the evolution of the metazoan genome are discussed.     

Characterization of active miniature inverted-repeat transposable elements in the peanut genome

Miniature inverted-repeat transposable elements (MITEs), some of which are known as active non-autonomous DNA transposons, are found in the genomes of plants and animals. In peanut (Arachis hypogaea), AhMITE1 has been identified in a gene for fatty-acid desaturase, and possessed excision activity. However, the AhMITE1 distribution and frequency of excision have not been determined for the peanut genome. In order to characterize AhMITE1s, their genomic diversity and transposition ability was investigated. Southern blot analysis indicated high AhMITE1 copy number in the genomes of A. hypogaea, A. magna and A. monticola, but not in A. duranensis. A total of 504 AhMITE1s were identified from the MITE-enriched genomic libraries of A. hypogaea. The representative AhMITE1s exhibited a mean length of 205.5 bp and a GC content of 30.1%, with AT-rich, 9 bp target site duplications and 25 bp terminal inverted repeats. PCR analyses were performed using primer pairs designed against both flanking sequences of each AhMITE1. These analyses detected polymorphisms at 169 out of 411 insertional loci in the four peanut lines. In subsequent analyses of 60 gamma-irradiated mutant lines, four AhMITE1 excisions showed footprint mutations at the 109 loci tested. This study characterizes AhMITE1s in peanut and discusses their use as DNA markers and mutagens for the genetics, genomics and breeding of peanut and its relatives.     

Marker utility of miniature inverted-repeat transposable elements for wheat biodiversity and evolution

Transposable elements (TEs) account for up to 80% of the wheat genome and are considered one of the main drivers of wheat genome evolution. However, the contribution of TEs to the divergence and evolution of wheat genomes is not fully understood. In this study, we have developed 55 miniature inverted-repeat transposable element (MITE) markers that are based on the presence/absence of an element, with over 60% of these 55 MITE insertions associated with wheat genes. We then applied these markers to assess genetic diversity among Triticum and Aegilops species, including diploid (AA, BB and DD genomes), tetraploid (BBAA genome) and hexaploid (BBAADD genome) species. While 18.2% of the MITE markers showed similar insertions in all species indicating that those are fossil insertions, 81.8% of the markers showed polymorphic insertions among species, subspecies, and accessions. Furthermore, a phylogenetic analysis based on MITE markers revealed that species were clustered based on genus, genome composition, and ploidy level, while 47.13% genetic divergence was observed between the two main clusters, diploids versus polyploids. In addition, we provide evidence for MITE dynamics in wild emmer populations. The use of MITEs as evolutionary markers might shed more light on the origin of the B-genome of polyploid wheat.     

Genome-wide analysis of mariner-like transposable elements in rice reveals complex relationships with stowaway miniature inverted repeat transposable elements (MITEs)

Stowaway is a superfamily of miniature inverted repeat transposable elements (MITEs) that is widespread and abundant in plant genomes. Like other MITEs, however, its origin and mode of amplification are poorly understood. Several lines of evidence point to plant mariner-like elements (MLEs) as the autonomous partners of the nonautonomous Stowaway MITEs. To better understand this relationship, we have taken advantage of the nearly complete genome sequences of two rice subspecies to generate the first inventory of virtually all MLEs and Stowaway families coexisting in a single plant species. Thirty-four different MLEs were found to group into three major clades and 25 families. More than 22,000 Stowaway MITEs were identified and classified into 36 families. On the basis of detailed sequence comparisons, MLEs were confirmed to be the best candidate autonomous elements for Stowaway MITEs. Surprisingly, however, sequence similarity between MLE and Stowaway families was restricted to the terminal inverted repeats (TIRs) and, in a few cases, to adjacent subterminal sequences. These data suggest a model whereby most of the Stowaway MITEs in rice were cross-mobilized by MLE transposases encoded by distantly related elements.     

Dynamic interactions between transposable elements and their hosts

Transposable elements (TEs) have a unique ability to mobilize to new genomic locations, and the major advance of second-generation DNA sequencing has provided insights into the dynamic relationship between TEs and their hosts. It now is clear that TEs have adopted diverse strategies - such as specific integration sites or patterns of activity - to thrive in host environments that are replete with mechanisms, such as small RNAs or epigenetic marks, that combat TE amplification. Emerging evidence suggests that TE mobilization might sometimes benefit host genomes by enhancing genetic diversity, although TEs are also implicated in diseases such as cancer. Here, we discuss recent findings about how, where and when TEs insert in diverse organisms.     

Plant transposable elements and their application in genetics and biotechnology

Data concerning plant transposable elements and their contribution to plant genome evolution are reviewed. Much attention is focused on utilization of transgenic plants as heterologous hosts of transposons for investigation of transposition mechanisms and gene cloning. Probable ways of the use of plant transposons as genetic tools in biotechnology are discussed.     

On the evolution and population genetics of hybrid-dysgenesis-causing transposable elements in Drosophila

Much has been learned about transposable genetic elements in Drosophila, but questions still remain, especially concerning their evolutionary significance. Three such questions are considered here. Has the behaviour of transposable elements been most influenced by natural selection at the level of the organism, the population, or the elements themselves? How did the elements originate in the genome of the species? Why are laboratory stocks different from natural populations with respect to their transposable element composition? No final answers to these questions are yet available, but by focusing on the two families of hybrid dysgenesis-causing elements, the P and I factors, we can draw some tentative conclusions.     

The structure of hobo transposable elements and their insertion sites

The hobo transposable elements of Drosophila form a family of 3.0-kb elements and their deletion derivatives. Their distribution is consistent with the model that 3.0-kb elements are functionally complete but that smaller hobos are defective and require complete elements in trans for transposition. The sequence of one 3.0-kb element is presented; it has several interesting features, including a 1.9-kb open reading frame downstream from potential TATA and CAT sequences. Comparison of 11 independent insertion sites shows that in every case the hobo element has integrated at and duplicated either the sequence NNNNNNAC or CTTTNNNN. There is evidence that an eight nucleotide sequence internal to hobo that matches both of these sequences has been used as an insertion site for a second hobo element, as the first step in the creation of an internal deletion derivative. Structural similarities between hobo and the eukaryotic transposable elements P, Ac, 1723, and Tam3, found in widely divergent host organisms, suggest that they all transpose by a common mechanism.     

Phylogenetic evidence for excision of Stowaway miniature inverted-repeat transposable elements in triticeae (Poaceae)

The mode of transposition of miniature inverted-repeat transposable elements (MITEs) is unknown, but it has been suggested that they are duplicated rather than excised at transposition. However, the present investigation demonstrates that a particular family of MITEs, Stowaway:, is excised. Mapped onto a gene tree based on partial sequences of disrupted meiotic cDNA1 (DMC1) from 30 species of the Triticeae grasses, it is evident that at least two excisions have occurred, leaving short footprints. These footprints may subsequently be reduced in length or deleted. Excision of Stowaway: elements lends strong support to the suggestion that MITEs are DNA transposons and should be classified as class II elements. The evolution of Stowaway: elements can also be traced by scrutiny of the gene tree. It appears that base substitutions are as frequent in the conserved terminal inverted repeats (TIRs) as in the core of the element. Neither substitutions nor deletions lead to compensatory changes; hence, the highly stable secondary structure of the elements may gradually be reduced.     

Population dynamics of miniature inverted-repeat transposable elements (MITEs) in Medicago truncatula

Miniature inverted-repeat transposable elements (MITEs) are small and high copy number transposons, related to and mobilized by some class II autonomous elements. New MITE families can be identified by computer-based mining of sequenced genomes. We describe four MITE families related to MtPH transposons mined de novo in the genome of Medicago truncatula, together with one previously described family MITRAV. Different levels of their intra-family sequence diversity and insertion polymorphism indicate that they were active at different evolutionary periods. MetMIT1 and MITRAV families were uniform in sequence and produced highly polymorphic insertion sites in 26 ecotypes representing a M. truncatula core collection. A subset of insertions was present only in the reference genome of A17 ‘Jemalong’, suggesting that the two families might have been active in the course of domestication. In contrast, all investigated insertions of the MetMIT2 family were fixed, showing that it was not active after M. truncatula speciation. MetMIT1 elements were divided into three clusters, i.e. (I) relatively heterogenous copies fixed in the genome of M. truncatula, (II) uniform but also mostly fixed, and (III) uniform and polymorphic among the investigated accessions. It might reflect the evolutionary history of the MetMIT1 family, showing multiple bursts of activity. A number of MetMIT1 and MITRAV insertions were present within 1 kb upstream or downstream the ORF. A high proportion of insertions proximal to coding regions was unique to A17 ‘Jemalong’.     

Repeat-induced point mutation and the population structure of transposable elements in Microbotryum violaceum

Repeat-induced point mutation (RIP) is a genome defense in fungi that hypermutates repetitive DNA and is suggested to limit the accumulation of transposable elements. The genome of Microbotryum violaceum has a high density of transposable elements compared to other fungi, but there is also evidence of RIP activity. This is the first report of RIP in a basidiomycete and was obtained by sequencing multiple copies of the integrase gene of a copia-type transposable element and the helicase gene of a Helitron-type element. In M. violaceum, the targets for RIP mutations are the cytosine residues of TCG trinucleotide combinations. Although RIP is a linkage-dependent process that tends to increase the variation among repetitive sequences, a chromosome-specific substructuring was observed in the transposable element population. The observed chromosome-specific patterns are not consistent with RIP, but rather suggest an effect of gene conversion, which is also a linkage-dependent process but results in a homogenization of repeated sequences. Particular sequences were found more widely distributed within the genome than expected by chance and may reflect the recently active variants. Therefore, sequence variation of transposable elements in M. violaceum appears to be driven by selection for transposition ability in combination with the context-specific forces of the RIP and gene conversion.     

Spring: a novel family of miniature inverted-repeat transposable elements is associated with genes in apple

The apple, Malusxdomestica Borkh., belongs to the family Rosaceae and subfamily Maloideae and has a genome size of approximately 750 Mb. In this study, a novel family of transposable elements, designated Spring, has been identified in the apple genome. The four Spring elements, Spring-1 to Spring-4, share all the classic features of miniature inverted-repeat transposable elements (MITEs), including small size (approximately 148 bp), no coding potential, A/T richness, insertion bias toward noncoding regions, terminal inverted repeats (TIRs), target site duplications, and potential for forming secondary structures. Evidence of previous mobility of Spring-4 is demonstrated by sequence alignment of genes encoding 1-aminocyclopropane-1-carboxylic acid synthase from both apple and a related member of the Maloideae subfamily, pear. The Spring elements are flanked by either 8- or 9-bp direct repeats, and they differ significantly in size compared to other previously reported MITEs in plants. The TIRs of these Spring elements are not found in any other previously reported plant genes or transposons, except for apple. The possible role of Spring elements in the apple genome is discussed.     

Characterization and potential evolutionary impact of transposable elements in the genome of Cochliobolus heterostrophus

Background

Cochliobolus heterostrophus is a dothideomycete that causes Southern Corn Leaf Blight disease. There are two races, race O and race T that differ by the absence (race O) and presence (race T) of ~ 1.2-Mb of DNA encoding genes responsible for the production of T-toxin, which makes race T much more virulent than race O. The presence of repetitive elements in fungal genomes is considered to be an important source of genetic variability between different species.

Results

A detailed analysis of class I and II TEs identified in the near complete genome sequence of race O was performed. In total in race O, 12 new families of transposons were identified. In silico evidence of recent activity was found for many of the transposons and analyses of expressed sequence tags (ESTs) demonstrated that these elements were actively transcribed. Various potentially active TEs were found near coding regions and may modify the expression and structure of these genes by acting as ectopic recombination sites. Transposons were found on scaffolds carrying polyketide synthase encoding genes, responsible for production of T-toxin in race T. Strong evidence of ectopic recombination was found, demonstrating that TEs can play an important role in the modulation of genome architecture of this species. The Repeat Induced Point mutation (RIP) silencing mechanism was shown to have high specificity in C. heterostrophus, acting only on transposons near coding regions.

Conclusions

New families of transposons were identified. In C. heterostrophus, the RIP silencing mechanism is efficient and selective. The co-localization of effector genes and TEs, therefore, exposes those genes to high rates of point mutations. This may accelerate the rate of evolution of these genes, providing a potential advantage for the host. Additionally, it was shown that ectopic recombination promoted by TEs appears to be the major event in the genome reorganization of this species and that a large number of elements are still potentially active. So, this study provides information about the potential impact of TEs on the evolution of C. heterostrophus.

Electronic supplementary material

The online version of this article (doi:10.1186/1471-2164-15-536) contains supplementary material, which is available to authorized users.     

Functional impact of transposable elements using bioinformatic analysis and a comparative genomic approach

A dual coding event, which is the translation of different isoforms from a single gene, is one of the special patterns among the alternative splicing events. This is an important mechanism for the regulation of protein diversity in human and mouse genomes. Although the regulation for dual coding events has been characterized in a few genes, the individual mechanism remains unclear. Numerous studies have described the exonization of transposable elements, which is the splicing mediated insertion of transposable element sequence fragments into mature mRNAs. Therefore, in this study, we investigated the number of transposable element (TE)-derived dual coding genes in human, chimpanzee and mouse genomes. TE fusion exons appeared in the dual coding regions of 309 human genes. Functional protein domain alterations by TE-derived dual coding events were observed in 129 human genes. Comparative TE-derived dual coding events were also analyzed in chimpanzee and mouse orthologs. Seventy chimpanzee orthologs had TE-derived dual coding events, but mouse orthologs did not have any TE-derived dual coding events. Taken together, our analyses listed the number of TE-derived dual coding genes which could be investigated by experimental analysis and suggested that TE-derived dual coding events were major sources for the functional diversity of human genes, but not mouse genes.     

Using rice to understand the origin and amplification of miniature inverted repeat transposable elements (MITEs)

Recent studies of rice miniature inverted repeat transposable elements (MITEs), largely fueled by the availability of genomic sequence, have provided answers to many of the outstanding questions regarding the existence of active MITEs, their source of transposases (TPases) and their chromosomal distribution. Although many questions remain about MITE origins and mode of amplification, data accumulated over the past two years have led to the formulation of testable models.     

Isolation, analysis and marker utility of novel miniature inverted repeat transposable elements from the barley genome

Four previously undescribed families of miniature inverted repeat transposable elements (MITEs) were isolated by searching barley genomic DNA using structure-based criteria. Putative MITEs were confirmed by PCR to determine their insertional polymorphism in a panel of diverse barley germplasm. Copy numbers for all these familes are somewhat low (less than 1,000 copies per family per haploid genome). In contrast to previous studies, a higher proportion of insertions of the new MITEs are found within known transposable elements (27%) than are associated with genes (15%). Preliminary studies were conducted on two of the new MITE families to test their utility as molecular markers. Insertional polymorphism levels for both the families are high and diversity trees produced by both the families are similar and congruent with known relationships among the germplasm studied, suggesting that both the MITE families are useful markers of barley genetic diversity.