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FARE, a new family of foldback transposons in Arabidopsis.

ABSTRACT: A new family of transposons, FARE, has been identified in Arabidopsis. The structure of these elements is typical of foldback transposons, a distinct subset of mobile DNA elements found in both plants and animals. The ends of FARE elements are long, conserved inverted repeat sequences typically 550 bp in length. These inverted repeats are modular in organization and are predicted to confer extensive secondary structure to the elements. FARE elements are present in high copy number, are heterogeneous in size, and can be divided into two subgroups. FARE1's average 1.1 kb in length and are composed entirely of the long inverted repeats. FARE2's are larger, up to 16.7 kb in length, and contain a large internal region in addition to the inverted repeat ends. The internal region is predicted to encode three proteins, one of which bears homology to a known transposase. FARE1.1 was isolated as an insertion polymorphism between the ecotypes Columbia and Nossen. This, coupled with the presence of 9-bp target-site duplications, strongly suggests that FARE elements have transposed recently. The termini of FARE elements and other foldback transposons are imperfect palindromic sequences, a unique organization that further distinguishes these elements from other mobile DNAs.

SUBMITTER: Windsor AJ

PROVIDER: S-EPMC1461375 | biostudies-other | 2000 Dec

REPOSITORIES: biostudies-other

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FARE, a new family of foldback transposons in Arabidopsis.

Windsor A J AJ Waddell C S CS

Genetics 20001201 4

A new family of transposons, FARE, has been identified in Arabidopsis. The structure of these elements is typical of foldback transposons, a distinct subset of mobile DNA elements found in both plants and animals. The ends of FARE elements are long, conserved inverted repeat sequences typically 550 bp in length. These inverted repeats are modular in organization and are predicted to confer extensive secondary structure to the elements. FARE elements are present in high copy number, are heterogen ...[more]

PMID: 11102389

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Project description:BackgroundA family of Tc1/mariner transposons with a characteristic DD38E triad of catalytic amino acid residues, named Intruder (IT), was previously discovered in sturgeon genomes, but their evolutionary landscapes remain largely unknown.ResultsHere, we comprehensively investigated the evolutionary profiles of ITs, and evaluated their cut-and-paste activities in cells. ITs exhibited a narrow taxonomic distribution pattern in the animal kingdom, with invasions into two invertebrate phyla (Arthropoda and Cnidaria) and three vertebrate lineages (Actinopterygii, Agnatha, and Anura): very similar to that of the DD36E/IC family. Some animal orders and species seem to be more hospitable to Tc1/mariner transposons, one order of Amphibia and seven Actinopterygian orders are the most common orders with horizontal transfer events and have been invaded by all four families (DD38E/IT, DD35E/TR, DD36E/IC and DD37E/TRT) of Tc1/mariner transposons, and eight Actinopterygii species were identified as the major hosts of these families. Intact ITs have a total length of 1.5-1.7 kb containing a transposase gene flanked by terminal inverted repeats (TIRs). The phylogenetic tree and sequence identity showed that IT transposases were most closely related to DD34E/Tc1. ITs have been involved in multiple events of horizontal transfer in vertebrates and have invaded most lineages recently (< 5 million years ago) based on insertion age analysis. Accordingly, ITs presented high average sequence identity (86-95%) across most vertebrate species, suggesting that some are putatively active. ITs can transpose in human HeLa cells, and the transposition efficiency of consensus TIRs was higher than that of the TIRs of natural isolates.ConclusionsWe conclude that DD38E/IT originated from DD34E/Tc1 and can be detected in two invertebrate phyla (Arthropoda and Cnidaria), and in three vertebrate lineages (Actinopterygii, Agnatha and Anura). IT has experienced multiple HT events in animals, dominated by recent amplifications in most species and has high identity among vertebrate taxa. Our reconstructed IT transposon vector designed according to the sequence from the "cat" genome showed high cut-and-paste activity. The data suggest that IT has been acquired recently and is active in many species. This study is meaningful for understanding the evolution of the Tc1/mariner superfamily members and their hosts.

Project description:BACKGROUND:"Domestication" of transposable elements (TEs) led to evolutionary breakthroughs such as the origin of telomerase and the vertebrate adaptive immune system. These breakthroughs were accomplished by the adaptation of molecular functions essential for TEs, such as reverse transcription, DNA cutting and ligation or DNA binding. Cryptons represent a unique class of DNA transposons using tyrosine recombinase (YR) to cut and rejoin the recombining DNA molecules. Cryptons were originally identified in fungi and later in the sea anemone, sea urchin and insects. RESULTS:Herein we report new Cryptons from animals, fungi, oomycetes and diatom, as well as widely conserved genes derived from ancient Crypton domestication events. Phylogenetic analysis based on the YR sequences supports four deep divisions of Crypton elements. We found that the domain of unknown function 3504 (DUF3504) in eukaryotes is derived from Crypton YR. DUF3504 is similar to YR but lacks most of the residues of the catalytic tetrad (R-H-R-Y). Genes containing the DUF3504 domain are potassium channel tetramerization domain containing 1 (KCTD1), KIAA1958, zinc finger MYM type 2 (ZMYM2), ZMYM3, ZMYM4, glutamine-rich protein 1 (QRICH1) and "without children" (WOC). The DUF3504 genes are highly conserved and are found in almost all jawed vertebrates. The sequence, domain structure, intron positions and synteny blocks support the view that ZMYM2, ZMYM3, ZMYM4, and possibly QRICH1, were derived from WOC through two rounds of genome duplication in early vertebrate evolution. WOC is observed widely among bilaterians. There could be four independent events of Crypton domestication, and one of them, generating WOC/ZMYM, predated the birth of bilaterian animals. This is the third-oldest domestication event known to date, following the domestication generating telomerase reverse transcriptase (TERT) and Prp8. Many Crypton-derived genes are transcriptional regulators with additional DNA-binding domains, and the acquisition of the DUF3504 domain could have added new regulatory pathways via protein-DNA or protein-protein interactions. CONCLUSIONS:Cryptons have contributed to animal evolution through domestication of their YR sequences. The DUF3504 domains are domesticated YRs of animal Crypton elements.

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FARE, a new family of foldback transposons in Arabidopsis.

Publications

FARE, a new family of foldback transposons in Arabidopsis.

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