Different strategies to persist: the pogo-like Lemi1 transposon produces miniature inverted-repeat transposable elements or typical defective elements in different plant genomes

Miniature inverted-repeat transposable elements (MITEs) are a particular type of defective class II elements present in genomes as high-copy-number populations of small and highly homogeneous elements. While virtually all class II transposon families contain non-autonomous defective transposon copies, only a subset of them have a related MITE family. At present it is not known in which circumstances MITEs are generated instead of typical class II defective transposons. The ability to produce MITEs could be an exclusive characteristic of particular transposases, could be related to a particular structure of certain defective class II elements, or could be the consequence of particular constraints imposed by certain host genomes on transposon populations. We describe here a new family of pogo-like transposons from Medicago truncatula closely related to the Arabidopsis Lemi1 element that we have named MtLemi1. In contrast to the Arabidopsis Lemi1, present as a single-copy element and associated with hundreds of related Emigrant MITEs, MtLemi1 has attained >30 copies and has not generated MITEs. This shows that a particular transposon can adopt completely different strategies to colonize genomes. The comparison of AtLemi1 and MtLemi1 reveals transposase-specific domains and possible regulatory sequences that could be linked to the ability to produce MITEs.     

Phylogenetic analysis reveals stowaway-like elements may represent a fourth family of the IS630-Tc1-mariner superfamily.

The genomes of plants, like virtually all other eukaryotic organisms, harbor a diverse array of mobile elements, or transposons. In terms of numbers, the predominant type of transposons in many plants is the miniature inverted-repeat transposable element (MITE). There are three archetypal MITEs, known as Tourist, Stowaway, and Emigrant, each of which can be defined by a specific terminal inverted-repeat (TIR) sequence signature. Although their presence was known for over a decade, only recently have open reading frames (ORFs) been identified that correspond to putative transposases for each of the archetypes. We have identified two Stowaway elements that encode a putative transposase and are similar to members of the previously characterized IS630-Tc1-mariner superfamily. In this report, we provide a high-resolution phylogenetic analysis of the evolutionary relationship between Stowaway, Emigrant, and members of the IS630-Tc1-mariner superfamily. We show that although Emigrant is closely related to the pogo-like family of elements, Stowaway may represent a novel family. Integration of our results with previously published data leads to the conclusion that the three main types of MITEs have different evolutionary histories despite similarity in structure.     

Amplification dynamics of miniature inverted-repeat transposable elements and their impact on rice trait variability

Transposable elements (TEs) are a rich source of genetic variability. Among TEs, miniature inverted-repeat TEs (MITEs) are of particular interest as they are present in high copy numbers in plant genomes and are closely associated with genes. MITEs are deletion derivatives of class II transposons, and can be mobilized by the transposases encoded by the latter through a typical cut-and-paste mechanism. However, MITEs are typically present at much higher copy numbers than class II transposons. We present here an analysis of 103 109 transposon insertion polymorphisms (TIPs) in 738 Oryza sativa genomes representing the main rice population groups. We show that an important fraction of MITE insertions has been fixed in rice concomitantly with its domestication. However, another fraction of MITE insertions is present at low frequencies. We performed MITE TIP-genome-wide association studies (TIP-GWAS) to study the impact of these elements on agronomically important traits and found that these elements uncover more trait associations than single nucleotide polymorphisms (SNPs) on important phenotypes such as grain width. Finally, using SNP-GWAS and TIP-GWAS we provide evidence of the replicative amplification of MITEs.     

Evidence that a family of miniature inverted-repeat transposable elements (MITEs) from the Arabidopsis thaliana genome has arisen from a pogo-like DNA transposon

Sequence similarities exist between terminal inverted repeats (TIRs) of some miniature inverted-repeat transposable element (MITE) families isolated from a wide range of organisms, including plants, insects, and humans, and TIRs of DNA transposons from the pogo family. We present here evidence that one of these MITE families, previously described for Arabidopsis thaliana, is derived from a larger element encoding a putative transposase. We have named this novel class II transposon Lemi1. We show that its putative product is related to transposases of the Tc1/mariner superfamily, being closer to the pogo family. A similar truncated element was found in a tomato DNA sequence, indicating an ancient origin and/or horizontal transfer for this family of elements. These results are reminiscent of those recently reported for the human genome, where other members of the pogo family, named Tiggers, are believed to be responsible for the generation of abundant MITE-like elements in an early primate ancestor. These results further suggest that some MITE families, which are highly reiterated in plant, insect, and human genomes, could have arisen from a similar mechanism, implicating pogo-like elements.     

植物中活性MITEs转座子研究进展

MITEs(Miniature inverted-repeat transposable elements)转座子是一种特殊的转座子,其既有DNA转座子的转座特性——"剪切-粘贴"转座方式,又有RNA转座子的高拷贝特性。目前已被报道的MITEs种类和数量虽然很多,但是关于有转座活性的MITEs的报道却甚少。本文总结了近几年来有关活性MITEs的相关报道,发现具有转座活性的MITEs种类大都分布在Tourist家族,分别是m Ping、m Ging、Ph Tourist1、Tmi1和Ph Tst-3,另外还有Stowaway-like家族的d Tstu1和MITE-39以及Mutator家族的Ah MITE1。文中还分析了这些活性MITEs的结构(TIR和TSD)、拷贝数、进化模式以及转座特性等,为鉴定其他活性MITEs以及MITEs转座和扩增机制的研究奠定了基础。     

Genome-wide analysis of the Emigrant family of MITEs of Arabidopsis thaliana

Miniature inverted-repeat transposable elements (MITEs) are structurally similar to defective class II elements, but their high copy number and the size and sequence conservation of most MITE families suggest that they can be amplified by a replicative mechanism. Here we present a genome-wide analysis of the Emigrant family of MITEs from Arabidopsis thaliana. In order to be able to detect divergent ancient copies, and low copy number subfamilies with a different internal sequence we have developed a computer program to look for Emigrant elements based solely on the terminal inverted-repeat sequence. We have detected 151 Emigrant elements of different subfamilies. Our results show that different bursts of amplification, probably of few active, or master, elements, have occurred at different times during Arabidopsis evolution. The analysis of the insertion sites of the Emigrant elements shows that recently inserted Emigrant elements tend to be located far from open reading frames, whereas more ancient Emigrant subfamilies are preferentially found associated to genes.     

Presence of miniature inverted-repeat transposable elements (MITEs) in the genome of Arabidopsis thaliana : characterisation of the Emigrant family of elements

Although the genome of Arabidopsis thaliana has a small amount of repetitive DNA, it contains representatives of most classes of mobile elements. However, to date, no miniature inverted-repeat transposable element (MITE) has been described in this plant. Here, we describe a new family of repeated sequences that we have named Emigrant , which are dispersed in the genome of Arabidopsi s and fulfil all the requirements of MITEs. These sequences are short, AT-rich, have terminal inverted repeats (TIRs), and do not seem to have any coding capacity. Evidence for the mobility of Emigrant elements has been obtained from the absence of one of these elements in a specific Arabidopsis ecotype. Emigrant is also present in the genome of different Brassicae and its TIRs are 74% identical to those of Wujin elements, a recently described family of MITEs from the yellow fever mosquito Aedes aegypti.      

Structural organization of the human gastrointestinal glutathione peroxidase (GPX2) promoter and 3'-nontranscribed region: transcriptional response to exogenous redox agents

We describe a new family of repetitive elements, named Mimo, from the mosquito Culex pipiens. Structural characteristics of these elements fit well with those of miniature inverted-repeat transposable elements (MITEs), which are ubiquitous and highly abundant in plant genomes. The occurrence of Mimo in C. pipiens provides new evidence that MITEs are not restricted to plant genomes, but may be widespread in arthropods as well. The copy number of Mimo elements in C. pipiens (1000 copies in a 540 Mb genome) supports the hypothesis that there is a positive correlation between genome size and the magnitude of MITE proliferation. In contrast to most MITE families described so far, members of the Mimo family share a high sequence conservation, which may reflect a recent amplification history in this species. In addition, we found that Mimo elements are a frequent nest for other MITE-like elements, suggesting that multiple and successive MITE transposition events have occurred very recently in the C. pipiens genome. Despite evidence for recent mobility of these MITEs, no element has been found to encode a protein; therefore, we do not know how they have transposed and have spread in the genome. However, some sequence similarities in terminal inverted-repeats suggest a possible filiation of some of these mosquito MITEs with pogo-like DNA transposons.     

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.     

MAK,a computational tool kit for automated MITE analysis

Miniature inverted repeat transposable elements (MITEs) are ubiquitous and numerous in higher eukaryotic genomes. Analysis of MITE families is laborious and time consuming, especially when multiple MITE families are involved in the study. Based on the structural characteristics of MITEs and genetic principles for transposable elements (TEs), we have developed a computational tool kit named MITE analysis kit (MAK) to automate the processes (http://perl.idmb.tamu.edu/mak.htm). In addition to its ability to routinely retrieve family member sequences and to report the positions of these elements relative to the closest neighboring genes, MAK is a powerful tool for revealing anchor elements that link MITE families to known transposable element families. Implementation of the MAK is described, as are genetic principles and algorithms used in its derivation. Test runs of the programs for several MITE families yielded anchor sequences that retain TIRs and coding regions reminiscent of transposases. These anchor sequences are consistent with previously reported putative autonomous elements for these MITE families. Furthermore, analysis of two MITE families with no known links to any transposon family revealed two novel transposon families, namely Math and Kid, belonging to the IS5/Harbinger/PIF superfamily.     

A sequence related to rice Pong transposable element displays transcriptional activation by in vitro culture and reveals somaclonal variations in maize.

Miniature inverted-repeat transposable elements (MITEs) are nonautonomous elements that are abundant in plant genomes. The rice MITE mPing was shown to be mobilized by anther culture, and the associated transposon Pong was shown to transpose actively in an Oryza sativa 'indica' rice cell-culture line. We have identified 3 sequences in maize named ZmTPAPong-like 1, 2, and 3 that displayed homology with the transposase of Pong. Here, we show that these sequences are differentially expressed during the in vitro androgenetic process in maize. We also demonstrate that the ZmTPAPong-like 1 and 3 sequences reveal somaclonal variations among plants regenerated from the calli of a doubled haploid line. These data suggest that the ZmTPAPong-like sequences could form part of a Zea mays element related to the rice Pong element. The possible activation of this newly discovered element under stress conditions is discussed.     

Recent amplification of miniature inverted-repeat transposable elements in the vector mosquito Culex pipiens: characterization of the Mimo family

We describe a new family of repetitive elements, named Mimo, from the mosquito Culex pipiens. Structural characteristics of these elements fit well with those of miniature inverted-repeat transposable elements (MITEs), which are ubiquitous and highly abundant in plant genomes. The occurrence of Mimo in C. pipiens provides new evidence that MITEs are not restricted to plant genomes, but may be widespread in arthropods as well. The copy number of Mimo elements in C. pipiens (1000 copies in a 540 Mb genome) supports the hypothesis that there is a positive correlation between genome size and the magnitude of MITE proliferation. In contrast to most MITE families described so far, members of the Mimo family share a high sequence conservation, which may reflect a recent amplification history in this species. In addition, we found that Mimo elements are a frequent nest for other MITE-like elements, suggesting that multiple and successive MITE transposition events have occurred very recently in the C. pipiens genome. Despite evidence for recent mobility of these MITEs, no element has been found to encode a protein; therefore, we do not know how they have transposed and have spread in the genome. However, some sequence similarities in terminal inverted-repeats suggest a possible filiation of some of these mosquito MITEs with pogo-like DNA transposons.     

The ancient mariner sails again: transposition of the human Hsmar1 element by a reconstructed transposase and activities of the SETMAR protein on transposon ends

Hsmar1, one of the two subfamilies of mariner transposons in humans, is an ancient element that entered the primate genome lineage approximately 50 million years ago. Although Hsmar1 elements are inactive due to mutational damage, one particular copy of the transposase gene has apparently been under selection. This transposase coding region is part of the SETMAR gene, in which a histone methylatransferase SET domain is fused to an Hsmar1 transposase domain. A phylogenetic approach was taken to reconstruct the ancestral Hsmar1 transposase gene, which we named Hsmar1-Ra. The Hsmar1-Ra transposase efficiently mobilizes Hsmar1 transposons by a cut-and-paste mechanism in human cells and zebra fish embryos. Hsmar1-Ra can also mobilize short inverted-repeat transposable elements (MITEs) related to Hsmar1 (MiHsmar1), thereby establishing a functional relationship between an Hsmar1 transposase source and these MITEs. MiHsmar1 excision is 2 orders of magnitude more efficient than that of long elements, thus providing an explanation for their high copy numbers. We show that the SETMAR protein binds and introduces single-strand nicks into Hsmar1 inverted-repeat sequences in vitro. Pathway choices for DNA break repair were found to be characteristically different in response to transposon cleavage mediated by Hsmar1-Ra and SETMAR in vivo. Whereas nonhomologous end joining plays a dominant role in repairing excision sites generated by the Hsmar1-Ra transposase, DNA repair following cleavage by SETMAR predominantly follows a homology-dependent pathway. The novel transposon system can be a useful tool for genome manipulations in vertebrates and for investigations into the transpositional dynamics and the contributions of these elements to primate genome evolution.     

A recently active miniature inverted-repeat transposable element, Chunjie, inserted into an operon without disturbing the operon structure in Geobacter uraniireducens Rf4

Miniature inverted-repeat transposable elements (MITEs) are short DNA transposons with terminal inverted repeat (TIR) signals and have been extensively studied in plants and other eukaryotes. But little is known about them in eubacteria. We identified a novel and recently active MITE, Chunjie, when studying the recent duplication of an operon consisting of ABC transporters and a phosphate uptake regulator in the chromosome of Geobacter uraniireducens Rf4. Chunjie resembles the other known MITEs in many aspects, e.g., having TIR signals and direct repeats, small in size, noncoding, able to fold into a stable secondary structure, and typically inserted into A + T-rich regions. At least one case of recent transposition was observed, i.e., the insertion of Chunjie into one copy of the aforementioned operon. As far as we know, this is the first report that the insertion of a MITE does not disrupt the operon structure.     

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.     

Short Inverted-Repeat Transposable Elements in Teleost Fish and Implications for a Mechanism of Their Amplification

Angel is the first miniature inverted-repeat transposable element (MITE) isolated from fish. Angel elements are imperfect palindromes with the potential to form stem-loop structures in vitro. Despite sequence divergence of elements of up to 55% within and between species, their inverted repeat structures have been maintained, implying functional importance. We estimate that there are about 10³–10⁴ Angels scattered throughout the zebrafish genome, evidence that this family of transposable elements has been significantly amplified over the course of evolution. Angel elements and Xenopus MITEs carry common sequence motifs at their termini, indicating common origin and/or related mechanisms of transposition. We present a model in which MITEs take advantage of the basic cellular mechanism of DNA replication for their amplification, which is dependent on the characteristic inverted repeat structures of these elements. We propose that MITEs are genomic parasites that transpose via a DNA intermediate, which forms by a folding-back of a single strand of DNA, that borrow all of the necessary factors for their amplification from products encoded in the genomes in which they reside. DNA polymorphisms in different lines of zebrafish were detected by PCR using Angel-specific primers, indicating that such elements, combined with other transposons in vertebrate genomes, will be useful molecular tools for genome mapping and genetic analyses of mutations. Received: 7 April 1998 / Accepted: 7 April 1998     

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.     

A new MITE family,Pangrangja, in Gramineae species

The miniature inverted-repeat transposable element (MITE) is a type of class II transposon. We have isolated a new MITE, Pangrangja, from the species Oryza. Although Pangrangja elements are present in a number of Gramineae species, they are more prevalent in A genome Oryza species, Triticum, Aegilops, Hordeum, and Tripsacum. The Pangrangja has a 16 bp terminal inverted repeat (TIR) and conserved trinucleotides 5'-TTG-3' and 5'-AAA-3' at both ends. The TIR starts with 5'-CAGT-3', similar to the MITEs of the Emigrant family. The sequences between TIRs are very AT-rich and vary in length from 161 bp in A genome Oryza species to 513 bp in Hordeum vulgare. While the size and sequence of Pangrangia elements are conserved in the A genome Oryza species, there is some sequence variation in other plants. In an analysis of the mobile history of Oryza sativa, eight RESites (related to empty sites) were found and grouped into three types depending on the presence or absence of the conserved trinucleotides 5'-TTG-3' and 5'-AAA-3'. Since one of the RESites showed a perfect palindromic 22 bp sequence into which 180 bp of the Pangrangja element was inserted, the possible role of secondary structure of the palindromic sequences is discussed. We also suggest that as Pangrangja MITE-AFLP has been successful in many different Gramineae, Pangrangja elements may be useful in the genomic analysis of grasses.     

<Emphasis Type="Italic">hATpin</Emphasis>, a Family of MITE-like <Emphasis Type="Italic">hAT</Emphasis> Mobile Elements Conserved in Diverse Plant Species that Forms Highly Stable Secondary Structures

We identified a 178 bp mobile DNA element in lettuce with characteristic CGAGC/GCTCG repeats in the subterminal regions. This element has terminal inverted repeats and 8-bp target site duplications typical of the hAT superfamily of class II mobile elements, but its small size and potential to form a single-stranded stable hairpin-like secondary structure suggest that it is related to MITE elements. In silico searches for related elements identified 252 plant sequences with 8-bp target site duplications and sequence similarity in their terminal and subterminal regions. Some of these sequences were predicted to encode transposases and may be autonomous elements; these constituted a separate clade within the phylogram of hAT transposases. We demonstrate that the CGAGC/GCTCG pentamer maximizes the hairpin stability compared to any other pentamer with the same C + G content, and the secondary structures of these elements are more stable than for most MITEs. We named these elements collectively as hATpin elements because of the hAT similarity and their hairpin structures. The nearly complete rice genome sequence and the highly advanced genome annotation allowed us to localize most rice elements and to deduce insertion preferences. hATpin elements are distributed on all chromosomes, but with significant bias for chromosomes 1 and 10 and in regions of moderate gene density. This family of class II mobile elements is found primarily in monocot species, but is also present in dicot species. Electronic supplementary material Electronic supplementary material is available for this article at and accessible for authorised users.