doi: 10.1073/pnas.151269298. Epub 2001 Jul 10.
Rolling-circle transposons in eukaryotes
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- PMID:11447285
- PMCID: PMC37501
- DOI: 10.1073/pnas.151269298
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Rolling-circle transposons in eukaryotes
V V Kapitonov et al. Proc Natl Acad Sci U S A..
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Abstract
All eukaryotic DNA transposons reported so far belong to a single category of elements transposed by the so-called "cut-and-paste" mechanism. Here, we report a previously unknown category of eukaryotic DNA transposons, Helitron, which transpose by rolling-circle replication. Autonomous Helitrons encode a 5'-to-3' DNA helicase and nuclease/ligase similar to those encoded by known rolling-circle replicons. Helitron-like transposons have conservative 5'-TC and CTRR-3' termini and do not have terminal inverted repeats. They contain 16- to 20-bp hairpins separated by 10--12 nucleotides from the 3'-end and transpose precisely between the 5'-A and T-3', with no modifications of the AT target sites. Together with their multiple diverged nonautonomous descendants, Helitrons constitute approximately 2% of both the Arabidopsis thaliana and Caenorhabditis elegans genomes and also colonize the Oriza sativa genome. Sequence conservation suggests that Helitrons continue to be transposed.
Figures
Reconstruction of theHelitron1 (A),Helitron2 (B), andHelitron1_CE (C) consensus sequences.The consensus sequences are schematically depicted as rectangles.Contiguous copies ofHelitrons that we used forreconstruction of the consensus sequences are shown as bold linesbeneath the rectangles. Gaps in the lines mark deletions ofcorresponding regions of the consensus sequences. GenBank accessionnos. and sequence coordinates are indicated. Genes and theircoordinates in the consensus sequences are indicated above therectangles. Genes coding for proteins composed of the Rep and helicasedomains are shaded in gray. The AT target sites are encircled.
Multiple alignment of helicases encoded by theHelitron1andHelitron1_CE transposons with a set of eukaryoticand prokaryotic DNA helicases. Domains I–VI that are conservative inDNA helicases from the SF1 superfamily (20) and distances between thesedomains are indicated. Domain IV/V has not been reported previously.Invariable positions are shaded in black, and those conserved in morethan 60% of the sequences are shaded in gray. The following are namesof helicases: PIF1 (GenBank protein identification no. 130196, yeast),BACULOVIRUS (7460536, the dsDNALymantia disparnucleopolyhedrovirus), CHILO (5725645, the dsDNA chilo iridescentvirus), TRAA_RHISN (2499024, a Ti-like plasmid fromRhizobium), TRAI_EC (136208, the F plasmid fromEscherichia coli), EXOV_EC (2507018, the RecD subunitfrom theE. coli exodeoxyribonuclease V), TRWC (1084124,the R388 conjugative plasmid fromE. coli), and HEL_T4(416895, the dsDNA T4 bacteriophage).
Termini ofHelitrons. Conserved 5′ and 3′ termini are inbold capital letters, 3′ terminal hairpins are shaded in gray, andinverted repeats are underlined.
Precise integration ofHelitrons into the host AT targetsites. Six insertion cases ofHelitrons (red) intodifferent transposons (green) are shown separately. Two copies ofATREP1, two copies ofHelitrony3_CE, and single copiesofHelitrony2_CE and ATREP9 are inserted into copiesof the ATTIRX1D, ATHATN1, PAL5A_CE, LTR2_CE, PALTTAA1_CE, andATREP10 transposons, respectively. The consensus sequences of theelements harboringHelitrons are marked by the boldblack letters and are described in theA. thaliana andC. elegans sections of Repbase Update atwww.girinst.org/Repbase_Update.html . Consensus sequences of thecorrespondingHelitrons are marked in blue. Asterisks,semicolons, and dots indicate identical nucleotide positions,transitions, and transversions, respectively. Only termini ofHelitrons are shown. Black, green, and blue numbers showpositions in the consensus sequences of the harboring transposons,GenBank, andHelitron consensus sequences,respectively.
Distributions of protein lengths predicted in 100 random DNA sequences.Every random sequence was 61% identical to ATRPA2H, without insertionsor deletions. Black marks all proteins predicted bygenscan ; gray marks proteins similar to ATRPA2Hp.
Alignment of the RC motifs in theHelitrons. Followingis a list of the RCR initiator-like proteins: SVTS2 (GenBank accessionno. AAF18310, the SVTS2 ssDNA spiroplasma plectrovirus); Rep_SC(BAA34784, the pSA1.1 conjugative plasmid fromStreptomycescyaneus); Rep_BB (BAA07788, the pHT926Bacillusborstelensis cryptic plasmid); Rep_AA (AAC37125, thepVT736–1 RCR plasmid fromActinobacillusactinomycetemcomitans); and Pf3 (AAA88392, the Pf3 ssDNAbacteriophage fromPseudomonas aeruginosa). Colorshading shows different physicochemical properties of conserved aminoacids (17). Conserved tyrosines, corresponding to the RCRnicking/ligation catalytic center, are marked by dots.
Comment in
- Treasures in the attic: rolling circle transposons discovered in eukaryotic genomes.Feschotte C, Wessler SR.Feschotte C, et al.Proc Natl Acad Sci U S A. 2001 Jul 31;98(16):8923-4. doi: 10.1073/pnas.171326198.Proc Natl Acad Sci U S A. 2001.PMID:11481459Free PMC article.No abstract available.
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