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. 2004 Feb;166(2):971–986. doi: 10.1534/genetics.166.2.971

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

Xiaoyu Zhang 1, Ning Jiang 1, Cédric Feschotte 1, Susan R Wessler 1
PMCID: PMC1470744  PMID: 15020481

Abstract

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.

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Selected References

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  1. Adey N. B., Schichman S. A., Graham D. K., Peterson S. N., Edgell M. H., Hutchison C. A., 3rd Rodent L1 evolution has been driven by a single dominant lineage that has repeatedly acquired new transcriptional regulatory sequences. Mol Biol Evol. 1994 Sep;11(5):778–789. doi: 10.1093/oxfordjournals.molbev.a040158. [DOI] [PubMed] [Google Scholar]
  2. Aparicio Samuel, Chapman Jarrod, Stupka Elia, Putnam Nik, Chia Jer-Ming, Dehal Paramvir, Christoffels Alan, Rash Sam, Hoon Shawn, Smit Arian. Whole-genome shotgun assembly and analysis of the genome of Fugu rubripes. Science. 2002 Jul 25;297(5585):1301–1310. doi: 10.1126/science.1072104. [DOI] [PubMed] [Google Scholar]
  3. Augé-Gouillou C., Hamelin M. H., Demattei M. V., Periquet M., Bigot Y. The wild-type conformation of the Mos-1 inverted terminal repeats is suboptimal for transposition in bacteria. Mol Genet Genomics. 2001 Mar;265(1):51–57. doi: 10.1007/s004380000385. [DOI] [PubMed] [Google Scholar]
  4. Benito M. I., Walbot V. Characterization of the maize Mutator transposable element MURA transposase as a DNA-binding protein. Mol Cell Biol. 1997 Sep;17(9):5165–5175. doi: 10.1128/mcb.17.9.5165. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Bennetzen Jeffrey L. Mechanisms and rates of genome expansion and contraction in flowering plants. Genetica. 2002 May;115(1):29–36. doi: 10.1023/a:1016015913350. [DOI] [PubMed] [Google Scholar]
  6. Bureau T. E., Ronald P. C., Wessler S. R. A computer-based systematic survey reveals the predominance of small inverted-repeat elements in wild-type rice genes. Proc Natl Acad Sci U S A. 1996 Aug 6;93(16):8524–8529. doi: 10.1073/pnas.93.16.8524. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Chen J., Greenblatt I. M., Dellaporta S. L. Transposition of Ac from the P locus of maize into unreplicated chromosomal sites. Genetics. 1987 Sep;117(1):109–116. doi: 10.1093/genetics/117.1.109. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Cresse A. D., Hulbert S. H., Brown W. E., Lucas J. R., Bennetzen J. L. Mu1-related transposable elements of maize preferentially insert into low copy number DNA. Genetics. 1995 May;140(1):315–324. doi: 10.1093/genetics/140.1.315. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Dietrich Charles R., Cui Feng, Packila Mark L., Li Jin, Ashlock Daniel A., Nikolau Basil J., Schnable Patrick S. Maize Mu transposons are targeted to the 5' untranslated region of the gl8 gene and sequences flanking Mu target-site duplications exhibit nonrandom nucleotide composition throughout the genome. Genetics. 2002 Feb;160(2):697–716. doi: 10.1093/genetics/160.2.697. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Feschotte Cédric, Jiang Ning, Wessler Susan R. Plant transposable elements: where genetics meets genomics. Nat Rev Genet. 2002 May;3(5):329–341. doi: 10.1038/nrg793. [DOI] [PubMed] [Google Scholar]
  11. Feschotte Cédric, Swamy Lakshmi, Wessler Susan R. Genome-wide analysis of mariner-like transposable elements in rice reveals complex relationships with stowaway miniature inverted repeat transposable elements (MITEs). Genetics. 2003 Feb;163(2):747–758. doi: 10.1093/genetics/163.2.747. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Feschotte Cédric, Wessler Susan R. Mariner-like transposases are widespread and diverse in flowering plants. Proc Natl Acad Sci U S A. 2001 Dec 26;99(1):280–285. doi: 10.1073/pnas.022626699. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Gilbert W., de Souza S. J., Long M. Origin of genes. Proc Natl Acad Sci U S A. 1997 Jul 22;94(15):7698–7703. doi: 10.1073/pnas.94.15.7698. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Goff Stephen A., Ricke Darrell, Lan Tien-Hung, Presting Gernot, Wang Ronglin, Dunn Molly, Glazebrook Jane, Sessions Allen, Oeller Paul, Varma Hemant. A draft sequence of the rice genome (Oryza sativa L. ssp. japonica). Science. 2002 Apr 5;296(5565):92–100. doi: 10.1126/science.1068275. [DOI] [PubMed] [Google Scholar]
  15. Hebsgaard S. M., Korning P. G., Tolstrup N., Engelbrecht J., Rouzé P., Brunak S. Splice site prediction in Arabidopsis thaliana pre-mRNA by combining local and global sequence information. Nucleic Acids Res. 1996 Sep 1;24(17):3439–3452. doi: 10.1093/nar/24.17.3439. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Jiang N., Wessler S. R. Insertion preference of maize and rice miniature inverted repeat transposable elements as revealed by the analysis of nested elements. Plant Cell. 2001 Nov;13(11):2553–2564. doi: 10.1105/tpc.010235. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Jiang Ning, Bao Zhirong, Zhang Xiaoyu, Hirochika Hirohiko, Eddy Sean R., McCouch Susan R., Wessler Susan R. An active DNA transposon family in rice. Nature. 2003 Jan 9;421(6919):163–167. doi: 10.1038/nature01214. [DOI] [PubMed] [Google Scholar]
  18. Jordan I. K., McDonald J. F. Evidence for the role of recombination in the regulatory evolution of Saccharomyces cerevisiae Ty elements. J Mol Evol. 1998 Jul;47(1):14–20. doi: 10.1007/pl00006358. [DOI] [PubMed] [Google Scholar]
  19. Kapitonov V. V., Jurka J. Molecular paleontology of transposable elements from Arabidopsis thaliana. Genetica. 1999;107(1-3):27–37. [PubMed] [Google Scholar]
  20. Kellogg E. A. Evolutionary history of the grasses. Plant Physiol. 2001 Mar;125(3):1198–1205. doi: 10.1104/pp.125.3.1198. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Kikuchi Kazuhiro, Terauchi Kazuki, Wada Masamitsu, Hirano Hiro-Yuki. The plant MITE mPing is mobilized in anther culture. Nature. 2003 Jan 9;421(6919):167–170. doi: 10.1038/nature01218. [DOI] [PubMed] [Google Scholar]
  22. Lampe D. J., Akerley B. J., Rubin E. J., Mekalanos J. J., Robertson H. M. Hyperactive transposase mutants of the Himar1 mariner transposon. Proc Natl Acad Sci U S A. 1999 Sep 28;96(20):11428–11433. doi: 10.1073/pnas.96.20.11428. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Le Q. H., Turcotte K., Bureau T. Tc8, a Tourist-like transposon in Caenorhabditis elegans. Genetics. 2001 Jul;158(3):1081–1088. doi: 10.1093/genetics/158.3.1081. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Lerat E., Brunet F., Bazin C., Capy P. Is the evolution of transposable elements modular? Genetica. 1999;107(1-3):15–25. [PubMed] [Google Scholar]
  25. Lisch Damon. Mutator transposons. Trends Plant Sci. 2002 Nov;7(11):498–504. doi: 10.1016/s1360-1385(02)02347-6. [DOI] [PubMed] [Google Scholar]
  26. Mahillon J., Chandler M. Insertion sequences. Microbiol Mol Biol Rev. 1998 Sep;62(3):725–774. doi: 10.1128/mmbr.62.3.725-774.1998. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Nakazaki Tetsuya, Okumoto Yutaka, Horibata Akira, Yamahira Satoshi, Teraishi Masayoshi, Nishida Hidetaka, Inoue Hiromo, Tanisaka Takatoshi. Mobilization of a transposon in the rice genome. Nature. 2003 Jan 9;421(6919):170–172. doi: 10.1038/nature01219. [DOI] [PubMed] [Google Scholar]
  28. Rezsöhazy R., Hallet B., Delcour J., Mahillon J. The IS4 family of insertion sequences: evidence for a conserved transposase motif. Mol Microbiol. 1993 Sep;9(6):1283–1295. doi: 10.1111/j.1365-2958.1993.tb01258.x. [DOI] [PubMed] [Google Scholar]
  29. Singer T., Yordan C., Martienssen R. A. Robertson's Mutator transposons in A. thaliana are regulated by the chromatin-remodeling gene Decrease in DNA Methylation (DDM1). Genes Dev. 2001 Mar 1;15(5):591–602. doi: 10.1101/gad.193701. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Tarchini R., Biddle P., Wineland R., Tingey S., Rafalski A. The complete sequence of 340 kb of DNA around the rice Adh1-adh2 region reveals interrupted colinearity with maize chromosome 4. Plant Cell. 2000 Mar;12(3):381–391. doi: 10.1105/tpc.12.3.381. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Tosi L. R., Beverley S. M. cis and trans factors affecting Mos1 mariner evolution and transposition in vitro, and its potential for functional genomics. Nucleic Acids Res. 2000 Feb 1;28(3):784–790. doi: 10.1093/nar/28.3.784. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Walker E. L., Eggleston W. B., Demopulos D., Kermicle J., Dellaporta S. L. Insertions of a novel class of transposable elements with a strong target site preference at the r locus of maize. Genetics. 1997 Jun;146(2):681–693. doi: 10.1093/genetics/146.2.681. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Wessler S. R., Bureau T. E., White S. E. LTR-retrotransposons and MITEs: important players in the evolution of plant genomes. Curr Opin Genet Dev. 1995 Dec;5(6):814–821. doi: 10.1016/0959-437x(95)80016-x. [DOI] [PubMed] [Google Scholar]
  34. Yu Jun, Hu Songnian, Wang Jun, Wong Gane Ka-Shu, Li Songgang, Liu Bin, Deng Yajun, Dai Li, Zhou Yan, Zhang Xiuqing. A draft sequence of the rice genome (Oryza sativa L. ssp. indica). Science. 2002 Apr 5;296(5565):79–92. doi: 10.1126/science.1068037. [DOI] [PubMed] [Google Scholar]
  35. Yu Z., Wright S. I., Bureau T. E. Mutator-like elements in Arabidopsis thaliana. Structure, diversity and evolution. Genetics. 2000 Dec;156(4):2019–2031. doi: 10.1093/genetics/156.4.2019. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Zhang L., Dawson A., Finnegan D. J. DNA-binding activity and subunit interaction of the mariner transposase. Nucleic Acids Res. 2001 Sep 1;29(17):3566–3575. doi: 10.1093/nar/29.17.3566. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Zhang X., Feschotte C., Zhang Q., Jiang N., Eggleston W. B., Wessler S. R. P instability factor: an active maize transposon system associated with the amplification of Tourist-like MITEs and a new superfamily of transposases. Proc Natl Acad Sci U S A. 2001 Oct 2;98(22):12572–12577. doi: 10.1073/pnas.211442198. [DOI] [PMC free article] [PubMed] [Google Scholar]

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