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  • Review Article
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Plant transposable elements: where genetics meets genomics

Nature Reviews Genetics volume 3, pages 329–341 (2002)Cite this article

Key Points

  • The analysis of unstable kernel phenotypes in maize led to the discovery and characterization of active class 2 DNA transposable elements (TEs).

  • These active elements are a very small fraction of the TEs found in plant genomes.

  • Access to all or part of the genomic sequence of an organism has led to the development of new techniques to analyse the life cycle of TEs and their interactions with the 'host' genome.

  • Two types of element — miniature inverted-repeat transposable elements (MITEs) and long terminal repeat (LTR) retrotransposons — predominate in plant genomes.

  • MITEs are non-autonomous class 2 elements, but most can now be connected with two superfamilies of transposases: Tc1/mariner and PIF/harbinger.

  • LTR retrotransposons are the single largest component of plant genomes and are responsible for the recent genome expansion in some plants.

  • Despite evidence of recent activity, TEs that are present in high copy numbers in plant genomes are almost universally found to be defective and/or epigenetically silenced.

  • Some LTR retrotransposons are transcriptionally activated by various biotic and abiotic stresses.

  • Availability of mutant backgrounds that are deficient in epigenetic regulation offers the promise of activating previously silenced TEs and revealing new facets of their biology.

Abstract

Transposable elements are the single largest component of the genetic material of most eukaryotes. The recent availability of large quantities of genomic sequence has led to a shift from the genetic characterization of single elements to genome-wide analysis of enormous transposable-element populations. Nowhere is this shift more evident than in plants, in which transposable elements were first discovered and where they are still actively reshaping genomes.

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Figure 1: Using kernel phenotypes to study transposon behaviour.
Figure 2: Model for the origin and amplification of MITEs.
Figure 3: Estimating the time of retrotransposon insertion.
Figure 4: Detection of new genomic insertions by transposon display.
Figure 5: Epigenetic silencing of transposable elements.

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References

  1. Lander, E. S. et al. Initial sequencing and analysis of the human genome. Nature 409, 860–921 (2001).

    CAS  PubMed  Google Scholar 

  2. SanMiguel, P. & Bennetzen, J. L. Evidence that a recent increase in maize genome size was caused by the massive amplification of intergene retrotransposons. Ann. Bot. 81, 37–44 (1998).

    Google Scholar 

  3. Vicient, C. M. et al. Retrotransposon BARE-1 and its role in genome evolution in the genus Hordeum. Plant Cell 11, 1769–1784 (1999).

    CAS  PubMed  PubMed Central  Google Scholar 

  4. Meyers, B. C., Tingey, S. V. & Morgante, M. Abundance, distribution, and transcriptional activity of repetitive elements in the maize genome. Genome Res. 11, 1660–1676 (2001).A detailed survey of maize retrotransposons that combines random genomic sample sequencing, hybridization to bacterial artificial chromosomes and data obtained from a large collection of ESTs.

    CAS  PubMed  PubMed Central  Google Scholar 

  5. McClintock, B. Chromosome organization and genic expression. Cold Spring Harbor Symp. Quant. Biol. 16, 13–47 (1951).

    CAS  PubMed  Google Scholar 

  6. Berg, D. E. & Howe, M. H. Mobile DNA (American Society for Microbiology Press, Washington, DC, 1989).

    Google Scholar 

  7. Wessler, S. R. Phenotypic diversity mediated by the maize transposable elements Ac and Spm. Science 242, 399–405 (1988).

    CAS  PubMed  Google Scholar 

  8. Fedoroff, N. in Mobile DNA (eds Berg, D. E. & Howe, M. M.) 375–411 (American Society for Microbiology Press, Washington, DC, 1989).

    Google Scholar 

  9. Craig, N. L., Craigie, R., Gellert, M. & Lambowitz, A. M. Mobile DNA II (American Society for Microbiology Press, Washington, DC, 2002).The newest edition of the transposable element bible.

    Google Scholar 

  10. McDonald, J. F. Transposable elements: possible catalysts of organismic evolution. Trends Ecol. Evol. 10, 123–126 (1995).

    CAS  PubMed  Google Scholar 

  11. Kidwell, M. G. & Lisch, D. Transposable elements as sources of variation in animals and plants. Proc. Natl Acad. Sci. USA. 94, 7704–7711 (1997).

    CAS  PubMed  PubMed Central  Google Scholar 

  12. Johns, M. A., Mottinger, J. & Freeling, M. A low copy number, copia-like transposon in maize. EMBO J. 4, 1093–1102 (1985).

    CAS  PubMed  PubMed Central  Google Scholar 

  13. Varagona, M. J., Purugganan, M. & Wessler, S. R. Alternative splicing induced by insertion of retrotransposons into the maize waxy gene. Plant Cell 4, 811–820 (1992).

    CAS  PubMed  PubMed Central  Google Scholar 

  14. Vignols, F., Rigau, J., Torres, M. A., Capellades, M. & Puigdomenech, P. The brown midrib3 (bm3) mutation in maize occurs in the gene encoding caffeic acid O methyltransferase. Plant Cell 7, 407–416 (1995).

    CAS  PubMed  PubMed Central  Google Scholar 

  15. Britten, R. J., Graham, D. E. & Neufeld, B. R. Analysis of repeating DNA sequences by reassociation kinetics. Methods Enzymol. 29, 363–405 (1974).

    CAS  PubMed  Google Scholar 

  16. Goldberg, R. B. DNA sequence organization in the soybean plant. Biochem. Genet. 16, 45–68 (1978).

    CAS  PubMed  Google Scholar 

  17. Singer, M. F. SINEs and LINEs: highly repeated short and long interspersed sequences in mammals. Cell 28, 433–434 (1982).

    CAS  PubMed  Google Scholar 

  18. Yoshioka, Y. et al. Molecular characterization of a short interspersed repetitive element from tobacco that exhibits sequence homology to specific tRNAs. Proc. Natl Acad. Sci. USA. 90, 6562–6566 (1993).

    CAS  PubMed  PubMed Central  Google Scholar 

  19. Leeton, P. R. J. & Smyth, D. R. An abundant LINE-like element amplified in the genome of Lilium speciosum. Mol. Gen. Genet. 237, 97–104 (1993).

    CAS  PubMed  Google Scholar 

  20. Bureau, T. E. & Wessler, S. R. Tourist: a large family of inverted-repeat elements frequently associated with maize genes. Plant Cell 4, 1283–1294 (1992).

    CAS  PubMed  PubMed Central  Google Scholar 

  21. Bureau, T. E. & Wessler, S. R. Stowaway: a new family of inverted-repeat elements associated with genes of both monocotyledonous and dicotyledonous plants. Plant Cell 6, 907–916 (1994).

    CAS  PubMed  PubMed Central  Google Scholar 

  22. 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. USA. 93, 8524–8529 (1996).

    CAS  PubMed  PubMed Central  Google Scholar 

  23. 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. 5, 814–821 (1995).

    CAS  PubMed  Google Scholar 

  24. Oosumi, T., Garlick, B. & Belknap, W. R. Identification of putative nonautonomous transposable elements associated with several transposon families in Caenorhabditis elegans. J. Mol. Evol. 43, 11–18 (1996).

    CAS  PubMed  Google Scholar 

  25. Tu, Z. Three novel families of miniature inverted-repeat transposable elements are associated with genes of the yellow fever mosquito, Aedes aegypti. Proc. Natl Acad. Sci. USA. 94, 7475–7480 (1997).

    CAS  PubMed  PubMed Central  Google Scholar 

  26. Tu, Z. Eight novel families of miniature inverted repeat transposable elements in the African malaria mosquito, Anopheles gambiae. Proc. Natl Acad. Sci. USA. 98, 1699–1704 (2001).This paper reports the use of new software (available at the author's web site – see links box) that is designed to rapidly identify MITEs on the basis of their structural characteristics.

    CAS  PubMed  PubMed Central  Google Scholar 

  27. Feschotte, C. & Mouchès, C. Recent amplification of miniature inverted-repeat transposable elements in the vector mosquito Culex pipiens: characterization of the Mimo. family. Gene 250, 109–116 (2000).

    CAS  PubMed  Google Scholar 

  28. Izsvak, Z. et al. Short inverted-repeat transposable elements in teleost fish and implications for a mechanism of their amplification. J. Mol. Evol. 48, 13–21 (1999).

    CAS  PubMed  Google Scholar 

  29. Unsal, K. & Morgan, G. T. A novel group of families of short interspersed repetitive elements (SINEs) in Xenopus: evidence of a specific target site for DNA-mediated transposition of inverted-repeat SINEs. J. Mol. Biol. 248, 812–823 (1995).

    CAS  PubMed  Google Scholar 

  30. Morgan, G. T. Identification in the human genome of mobile elements spread by DNA-mediated transposition. J. Mol. Biol. 254, 1–5 (1995).

    CAS  PubMed  Google Scholar 

  31. Smit, A. F. A. & Riggs, A. D. Tiggers and DNA transposon fossils in the human genome. Proc. Natl Acad. Sci. USA. 93, 1443–1448 (1996).

    CAS  PubMed  PubMed Central  Google Scholar 

  32. The Arabidopsis Genome Initiative. Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature 408, 796–815 (2000).

  33. Turcotte, K., Srinivasan, S. & Bureau, T. Survey of transposable elements from rice genomic sequences. Plant J. 25, 169–179 (2001).

    CAS  PubMed  Google Scholar 

  34. 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 13, 2553–2564 (2001).

    CAS  PubMed  PubMed Central  Google Scholar 

  35. Zhang, Q., Arbuckle, J. & Wessler, S. R. Recent, extensive and preferential insertion of members of the miniature inverted-repeat transposable element family Heartbreaker. (Hbr) into genic regions of maize. Proc. Natl Acad. Sci. USA. 97, 1160–1165 (2000).

    CAS  PubMed  PubMed Central  Google Scholar 

  36. Feschotte, C., Zhang, X. & Wessler, S. R. in Mobile DNA II (eds Craig, N. L., Craigie, R., Gellert, M. & Lambowitz, A. M.) (American Society of Microbiology Press, Washington, DC, in the press).

  37. Feschotte, C. & Mouchès, C. Evidence that a family of miniature inverted-repeat transposable elements (MITEs) from the Arabidopsis thaliana genome has arisen from a pogo-like DNA transposon. Mol. Biol. Evol. 17, 730–737 (2000).

    CAS  PubMed  Google Scholar 

  38. Feschotte, C. & Wessler, S. R. Mariner-like transposases are widespread and diverse in flowering plants. Proc. Natl Acad. Sci. USA. 99, 280–285 (2002).Database searches and PCR experiments with plant-specific degenerate primers were combined to show that mariner -like TEs have successfully colonized many angiosperm genomes.

    CAS  PubMed  Google Scholar 

  39. 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 146, 681–693 (1997).

    CAS  PubMed  PubMed Central  Google Scholar 

  40. Zhang, X. et al. 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. USA. 98, 12572–12577 (2001).Reports the first connection between an active maize DNA transposon system and a Tourist -like MITE family. Here, a 'top-down' approach was used in the isolation of an element that is required for transpositional activity and the identification of a new superfamily of eukaryotic transposases.

    CAS  PubMed  PubMed Central  Google Scholar 

  41. Kapitonov, V. V. & Jurka, J. Molecular paleontology of transposable elements from Arabidopsis thaliana. Genetica 107, 27–37 (1999).

    CAS  PubMed  Google Scholar 

  42. Le, Q. H., Turcotte, K. & Bureau, T. Tc8, a Tourist-like transposon in Caenorhabditis elegans. Genetics 158, 1081–1088 (2001).

    CAS  PubMed  PubMed Central  Google Scholar 

  43. Engels, W. R., Johnson-Schlitz, D. M., Eggleston, W. B. & Sved, J. High-frequency P element loss in Drosophila is homolog dependent. Cell 62, 515–525 (1990).

    CAS  PubMed  Google Scholar 

  44. Rubin, E. & Levy, A. A. Abortive gap repair: underlying mechanism for Ds element formation. Mol. Cell. Biol. 17, 6294–6302 (1997).

    CAS  PubMed  PubMed Central  Google Scholar 

  45. Casacuberta, E., Casacuberta, J. M., Puigdomenech, P. & Monfort, A. Presence of miniature inverted-repeat transposable elements (MITEs) in the genome of Arabidopsis thaliana: characterisation of the Emigrant family of elements. Plant J. 16, 79–85 (1998).

    CAS  PubMed  Google Scholar 

  46. Wessler, S. R., Nagel, A. & Casa, A. M. in Proceedings of the Fourth International Rice Genetics Symposium. (eds Khush, G. S., Brar, D. S. & Hardy, B.) 107–116 (International Rice Research Institute, Los Baños, the Philippines, 2001).

    Google Scholar 

  47. Casa, A. M. et al. The MITE family heartbreaker (Hbr): molecular markers in maize. Proc. Natl Acad. Sci. USA. 97, 10083–10089 (2000).

    CAS  PubMed  PubMed Central  Google Scholar 

  48. Casa, A. M. et al. Evaluation of Hbr. (MITE) markers for assessment of genetic relationships among maize (Zea mays. L.) inbred lines. Theor. Appl. Genet. 104, 104–110 (2002).

    CAS  PubMed  Google Scholar 

  49. Kumar, A. & Bennetzen, J. L. Plant retrotransposons. Annu. Rev. Genet. 33, 479–532 (1999).

    CAS  PubMed  Google Scholar 

  50. Grandbastien, M.-A., Spielmann, A. & Caboche, M. Tnt1, a mobile retroviral-like transposable element of tobacco isolated by plant cell genetics. Nature 337, 376–380 (1989).

    CAS  PubMed  Google Scholar 

  51. Hirochika, H. et al. Autonomous transposition of the tobacco retrotransposon Tto1 in rice. Plant Cell 8, 725–734 (1996).

    CAS  PubMed  PubMed Central  Google Scholar 

  52. Marillonnet, S. & Wessler, S. R. Extreme structural heterogeneity among the members of a maize retrotransposon family. Genetics 150, 1245–1256 (1998).

    CAS  PubMed  PubMed Central  Google Scholar 

  53. Joseph, J. L., Sentry, J. W. & Smyth, D. R. Interspecies distribution of abundant DNA sequences in Lilium. J. Mol. Evol. 30, 146–154 (1990).

    CAS  Google Scholar 

  54. Thomas, C. A. The genetic organization of chromosomes. Annu. Rev. Genet. 5, 237–256 (1971).

    CAS  PubMed  Google Scholar 

  55. SanMiguel, P. et al. Nested retrotransposons in the intergenic regions of the maize genome. Science 274, 765–768 (1996).

    CAS  PubMed  Google Scholar 

  56. SanMiguel, P., Gaut, B. S., Tikhonov, A., Nakajima, Y. & Bennetzen, J. L. The paleontology of intergene retrotransposons of maize. Nature Genet. 20, 43–45 (1998).References 55 and 56 show that LTR retrotransposons make up more than half of the maize genome and that amplification of several families is responsible for doubling the genome in the past 5–6 million years.

    CAS  PubMed  Google Scholar 

  57. Kalendar, R., Tanskanen, J., Immonen, S., Nevo, E. & Schulman, A. H. Genome evolution of wild barley (Hordeum spontaneum) by BARE-1 retrotransposon dynamics in response to sharp microclimatic divergence. Proc. Natl Acad. Sci. USA. 97, 6603–6607 (2000).Along with reference 3 , this study documents large variations in the copy number of BARE-1 retrotransposons among and within Hordeum . species. By correlating this variation with intraspecific variation in genome size and with local changes in environmental conditions, the authors suggest that TE-mediated alterations might be adaptive.

    CAS  PubMed  PubMed Central  Google Scholar 

  58. Sassaman, D. M. et al. Many human L1 elements are capable of retrotransposition. Nature Genet. 16, 37–43 (1997).

    CAS  PubMed  Google Scholar 

  59. Pouteau, S., Grandbastien, M. A. & Boccara, M. Microbial elicitors of plant defense responses activate transcription of a retrotransposon. Plant J. 5, 535–542 (1994).

    CAS  Google Scholar 

  60. Hirochika, H. Activation of tobacco retrotransposons during tissue culture. EMBO J. 12, 2521–2528 (1993).

    CAS  PubMed  PubMed Central  Google Scholar 

  61. Hirochika, H., Sugimoto, K., Otsuki, Y. & Kanda, M. Retrotransposons of rice involved in mutations induced by tissue culture. Proc. Natl Acad. Sci. USA. 93, 7783–7788 (1996).

    CAS  PubMed  PubMed Central  Google Scholar 

  62. Grandbastien, M.-A. Activation of plant retrotransposons under stress conditions. Trends Plant Sci. 3, 181–189 (1998).

    Google Scholar 

  63. Curcio, M. J. & Garfinkel, D. J. New lines of host defense: inhibition of Ty1 retrotransposition by Fus3p and NER/TFIIH. Trends Genet. 15, 43–45 (1999).

    CAS  PubMed  Google Scholar 

  64. Melayah, D., Bonnivard, E., Chalhoub, B., Audeon, C. & Grandbastien, M. A. The mobility of the tobacco Tnt1 retrotransposon correlates with its transcriptional activation by fungal factors. Plant J. 28, 159–168 (2001).Illustrates the use of transposon display to detect de novo insertions of a moderately high-copy-number retrotransposon following stress induction.

    CAS  PubMed  Google Scholar 

  65. Waugh, R. et al. Genetic distribution of BARE1 retrotransposable elements in the barley genome revealed by sequence-specific amplification polymorphisms (S-SAP). Mol. Gen. Genet. 253, 687–694 (1997).

    CAS  PubMed  Google Scholar 

  66. Suoniemi, A., Narvanto, A. & Schulman, A. H. The BARE-1 retrotransposon is transcribed in barley from an LTR promoter active in transient assays. Plant Mol. Biol. 31, 295–306 (1996).

    CAS  PubMed  Google Scholar 

  67. Jaaskelainen, M. et al. Retrotransposon BARE-1: expression of encoded proteins and formation of virus-like particles in barley cells. Plant J. 20, 413–422 (1999).

    CAS  PubMed  Google Scholar 

  68. Kimura, Y. et al. OARE-1, a Ty1-copia retrotransposon in oat activated by abiotic and biotic stresses. Plant Cell Physiol. 42, 1345–1354 (2001).

    CAS  PubMed  Google Scholar 

  69. McClintock, B. The Suppressor–Mutator system of control of gene action in maize. Carnegie Inst. Wash. Yearb. 57, 415–429 (1958).

    Google Scholar 

  70. McClintock, B. Components of action of the regulators Spm and Ac. Carnegie Inst. Wash. Yearb. 64, 527–534 (1965).

    Google Scholar 

  71. Chandler, V. L. & Walbot, V. DNA modification of a maize transposable element correlates with loss of activity. Proc. Natl Acad. Sci. USA. 83, 1767–1771 (1986).

    CAS  PubMed  PubMed Central  Google Scholar 

  72. Chomet, P., Wessler, S. R. & Dellaporta, S. L. Inactivation of the maize transposable element Activator. is associated with its DNA modification. EMBO J. 6, 295–302 (1987).

    CAS  PubMed  PubMed Central  Google Scholar 

  73. Banks, J. A., Masson, P. & Fedoroff, N. Molecular mechanisms in the developmental regulation of the maize Suppressor–Mutator transposable element. Genes Dev. 2, 1364–1380 (1988).

    CAS  PubMed  Google Scholar 

  74. Li, E., Bestor, T. H. & Jaenisch, R. Targeted mutation of the DNA methyltransferase gene results in embryonic lethality. Cell 69, 915–926 (1992).

    CAS  PubMed  Google Scholar 

  75. Kakutani, T., Jeddeloh, J. A., Flowers, S. K., Munakata, K. & Richards, E. J. Developmental abnormalities and epimutations associated with DNA hypomethylation mutations. Proc. Natl Acad. Sci. USA. 93, 12406–12411 (1996).

    CAS  PubMed  PubMed Central  Google Scholar 

  76. Bestor, T. H. DNA methylation: evolution of a bacterial immune function into a regulator of gene expression and genome structure in higher eukaryotes. Phil. Trans. R. Soc. Lond. B Biol. Sci. 326, 179–187 (1990).

    CAS  Google Scholar 

  77. Flavell, R. B. Inactivation of gene expression in plants as a consequence of specific sequence duplication. Proc. Natl Acad. Sci. USA. 91, 3490–3496 (1994).

    CAS  PubMed  PubMed Central  Google Scholar 

  78. Voinnet, O. RNA silencing as a plant immune system against viruses. Trends Genet. 17, 449–459 (2001).

    CAS  PubMed  Google Scholar 

  79. Vaucheret, H. & Fagard, M. Transcriptional gene silencing in plants: targets, inducers and regulators. Trends Genet. 17, 29–35 (2001).

    CAS  PubMed  Google Scholar 

  80. Matzke, M. A., Matzke, A. J., Pruss, G. J. & Vance, V. B. RNA-based silencing strategies in plants. Curr. Opin. Genet. Dev. 11, 221–227 (2001).

    CAS  PubMed  Google Scholar 

  81. Jeong, B. R., Wu-Scharf, D., Zhang, C. & Cerutti, H. Suppressors of transcriptional transgenic silencing in Chlamydomonas are sensitive to DNA-damaging agents and reactivate transposable elements. Proc. Natl Acad. Sci. USA. 99, 1076–1081 (2002).

    CAS  PubMed Central  Google Scholar 

  82. 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. 15, 591–602 (2001).

    CAS  PubMed  PubMed Central  Google Scholar 

  83. Miura, A. et al. Mobilization of transposons by a mutation abolishing full DNA methylation in Arabidopsis. Nature 411, 212–214 (2001).

    CAS  PubMed  Google Scholar 

  84. Hirochika, H., Okamoto, H. & Kakutani, T. Silencing of retrotransposons in Arabidopsis and reactivation by the ddm1 mutation. Plant Cell 12, 357–369 (2000).

    CAS  PubMed  PubMed Central  Google Scholar 

  85. Wright, D. A. & Voytas, D. F. Athila4 of Arabidopsis and calypso of soybean define a lineage of endogenous plant retroviruses. Genome Res. 12, 122–131 (2002).References 82–85 show that a subset of Arabidopsis retrotransposons and DNA transposons are transcriptionally regulated by the SWI2/SNF2 chromatin-remodelling factor DDM1.

    CAS  PubMed  PubMed Central  Google Scholar 

  86. Jeddeloh, J. A., Stokes, T. L. & Richards, E. J. Maintenance of genomic methylation requires a SWI2/SNF2-like protein. Nature Genet. 22, 94–97 (1999).

    CAS  PubMed  Google Scholar 

  87. Jin, Y. K. & Bennetzen, J. L. Structure and coding properties of Bs1, a maize retrovirus-like transposon. Proc. Natl Acad. Sci. USA. 86, 6235–6239 (1989).

    CAS  PubMed  PubMed Central  Google Scholar 

  88. Jiang, N. et al. Dasheng: a recently amplified non-autonomous LTR element that is a major component of pericentromeric regions in rice. Genetics (in the press).

  89. Witte, C. P., Le, Q. H., Bureau, T. & Kumar, A. Terminal-repeat retrotransposons in miniature (TRIM) are involved in restructuring plant genomes. Proc. Natl Acad. Sci. USA. 98, 13778–13783 (2001).

    CAS  PubMed  PubMed Central  Google Scholar 

  90. Ogiwara, I., Miya, M., Ohshima, K. & Okada, N. Retropositional parasitism of SINEs on LINEs: identification of SINEs and LINEs in elasmobranchs. Mol. Biol. Evol. 16, 1238–1250 (1999).

    CAS  PubMed  Google Scholar 

  91. Kapitonov, V. V. & Jurka, J. Rolling-circle transposons in eukaryotes. Proc. Natl Acad. Sci. USA. 98, 8714–8719 (2001).

    CAS  PubMed  PubMed Central  Google Scholar 

  92. Lampe, D. J., Churchill, M. E. & Robertson, H. M. A purified mariner transposase is sufficient to mediate transposition in vitro. EMBO J. 15, 5470–5479 (1996).

    CAS  PubMed  PubMed Central  Google Scholar 

  93. Ivics, Z., Hackett, P. B., Plasterk, R. H. & Izsvak, Z. Molecular reconstruction of Sleeping Beauty, a Tc1-like transposon from fish, and its transposition in human cells. Cell 91, 501–510 (1997).References 92 and 93 emphasize the power of phylogenetic analyses to reconstruct an active transposase from a subset of inactive TE copies. Following these breakthrough studies, the reconstructed elements have been further developed into efficient transformation and mutagenic tools for a wide range of organisms.

    CAS  PubMed  Google Scholar 

  94. Jordan, I. K. & McDonald, J. F. Comparative genomics and evolutionary dynamics of Saccharomyces cerevisiae Ty elements. Genetica 107, 3–13 (1999).

    CAS  PubMed  Google Scholar 

  95. Lerat, E., Brunet, F., Bazin, C. & Capy, P. Is the evolution of transposable elements modular? Genetica 107, 15–25 (1999).

    CAS  PubMed  Google Scholar 

  96. Malik, H. S. & Eickbush, T. H. Phylogenetic analysis of ribonuclease H domains suggests a late, chimeric origin of LTR retrotransposable elements and retroviruses. Genome Res. 11, 1187–1197 (2001).

    CAS  PubMed  Google Scholar 

  97. Bowen, N. J. & McDonald, J. F. Drosophila euchromatic LTR retrotransposons are much younger than the host species in which they reside. Genome Res. 11, 1527–1540 (2001).

    CAS  PubMed  PubMed Central  Google Scholar 

  98. Schwarz-Sommer, Z., Le Clercq, L., Gobel, E. & Saedler, H. Cin4, an insert altering the structure of the A1 gene in Zea mays, exhibits properties of nonviral retrotransposons. EMBO J. 6, 3873–3880 (1987).

    CAS  PubMed  PubMed Central  Google Scholar 

  99. Wright, D. et al. Multiple non-LTR retrotransposons in the genome of Arabidopsis thaliana. Genetics 142, 569–578 (1996).

    CAS  PubMed  PubMed Central  Google Scholar 

  100. Deragon, J. M. et al. An analysis of retroposition in plants based on a family of SINEs from Brassica napus. J. Mol. Evol. 39, 378–386 (1994).

    CAS  PubMed  Google Scholar 

  101. White, S. E., Habera, L. F. & Wessler, S. R. Retrotransposons in the flanking regions of normal plant genes: a role for copia-like elements in the evolution of gene structure and expression. Proc. Natl Acad. Sci. USA. 91, 11792–11796 (1994).

    CAS  PubMed  PubMed Central  Google Scholar 

  102. Purugganan, M. D. & Wessler, S. R. Molecular evolution of magellan, a maize Ty3/gypsy-like retrotransposon. Proc. Natl Acad. Sci. USA. 91, 11674–11678 (1994).

    CAS  PubMed  PubMed Central  Google Scholar 

  103. Konieczny, A., Voytas, D. F., Cummings, M. P. & Ausubel, F. M. A superfamily of Arabidopsis thaliana retrotransposons. Genetics 127, 801–809 (1991).

    CAS  PubMed  PubMed Central  Google Scholar 

  104. Gierl, A. The En/Spm transposable element of maize. Curr. Top. Microbiol. Immunol. 204, 145–159 (1996).

    CAS  PubMed  Google Scholar 

  105. Chandler, V., Rivin, C. & Walbot, V. Stable non-mutator stocks of maize have sequences homologous to the Mu1 transposable element. Genetics 114, 1007–1021 (1986).

    CAS  PubMed  PubMed Central  Google Scholar 

  106. Parsons, J. D. Miropeats: graphical DNA sequence comparisons. Comput. Appl. Biosci. 11, 615–619 (1995).

    CAS  PubMed  Google Scholar 

  107. Kurtz, S. & Schleiermacher, C. REPuter: fast computation of maximal repeats in complete genomes. Bioinformatics 15, 426–427 (1999).

    CAS  PubMed  Google Scholar 

  108. Jurka, J. Repbase update: a database and an electronic journal of repetitive elements. Trends Genet. 16, 418–420 (2000).

    CAS  PubMed  Google Scholar 

  109. Lindroth, A. M. et al. Requirement of CHROMOMETHYLASE3 for maintenance of CpXpG methylation. Science 292, 2077–2080 (2001).

    CAS  PubMed  Google Scholar 

  110. Tompa, R. et al. Genome-wide profiling of DNA methylation reveals transposon targets of CHROMOMETHYLASE3. Curr. Biol. 12, 65–68 (2002).A new microarray technique for genome-wide mapping of cytosine methylation reveals that various retrotransposons are the preferential targets of CpNpG methylation in Arabidopsis.

    CAS  PubMed  Google Scholar 

  111. Steimer, A. et al. Endogenous targets of transcriptional gene silencing in Arabidopsis. Plant Cell 12, 1165–1178 (2000).

    CAS  PubMed  PubMed Central  Google Scholar 

  112. Amedeo, P., Habu, Y., Afsar, K., Scheid, O. M. & Paszkowski, J. Disruption of the plant gene MOM releases transcriptional silencing of methylated genes. Nature 405, 203–206 (2000).

    CAS  PubMed  Google Scholar 

  113. Ketting, R. F., Haverkamp, T. H., Van Luenen, H. G. & Plasterk, R. H. Mut-7 of C. elegans, required for transposon silencing and RNA interference, is a homolog of Werner syndrome helicase and RNaseD. Cell 99, 133–141 (1999).

    CAS  PubMed  Google Scholar 

  114. Wu-Scharf, D., Jeong, B., Zhang, C. & Cerutti, H. Transgene and transposon silencing in Chlamydomonas reinhardtii. by a DEAH-box RNA helicase. Science 290, 1159–1162 (2000).This paper and reference 81 show that the silencing of a DNA transposon and a LTR retrotransposon in Chlamydomonas involve enzymatic components of both PTGS and TGS, but do not seem to require DNA methylation.

    CAS  PubMed  Google Scholar 

  115. Aravin, A. A. et al. Double-stranded RNA-mediated silencing of genomic tandem repeats and transposable elements in the D. melanogaster germline. Curr. Biol. 11, 1017–1027 (2001).

    CAS  PubMed  Google Scholar 

  116. Jensen, S., Gassama, M. P. & Heidmann, T. Taming of transposable elements by homology-dependent gene silencing. Nature Genet. 21, 209–212 (1999).

    CAS  PubMed  Google Scholar 

  117. Djikeng, A., Shi, H., Tschudi, C. & Ullu, E. RNA interference in Trypanosoma brucei: cloning of small interfering RNAs provides evidence for retroposon-derived 24–26-nucleotide RNAs. RNA 7, 1522–1530 (2001).

    CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

We thank members of the Wessler lab, Z. Bao and E. Pritham for suggestions on the manuscript and stimulating discussions, and H. Cerrutti, S. Eddy, M.-A. Grandbastien, R. Martienssen, J. Tu and D. Voytas for providing helpful information and unpublished data. This work was supported by grants from the National Science Foundation (Plant Genome Initiative), the National Institute of Health, the Department of Energy and the University of Georgia Research Foundation to S.R.W.

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Authors and Affiliations

  1. Departments of Plant Biology and Genetics, The University of Georgia, Athens, 30602, Georgia, USA

    Cédric Feschotte, Ning Jiang & Susan R. Wessler

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  1. Cédric Feschotte
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  2. Ning Jiang
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  3. Susan R. Wessler
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Correspondence to Susan R. Wessler.

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DATABASES

MaizeDB

Ac

adh1

Bs1

Ds

Hopscotch

Huck-2

Magellan

Mutator

Opie-2

Spm

Stonor

Stowaway

Tourist

The <i>Arabidopsis</i> Information Resource

ddm1

FURTHER INFORMATION

Encyclopedia of Life Sciences

Repetitive DNA: evolution

Transposons; eukaryotic

Barbara McClintock

Sue Wessler's lab

Zhijian Tu's web page

Glossary

ENDOSPERM

A triploid nutritive tissue in flowering plants.

EPIGENETIC

Any heritable change in gene expression that is not caused by a change in DNA sequence.

ORTHOLOGOUS GENES

Homologous genes that originated through speciation (for example, human and mouse β-globin).

PARALOGOUS GENES

Homologous genes that originated by gene duplication (for example, human α-globin and β-globin).

ABORTIVE GAP REPAIR

The double-stranded DNA break left at the site of excision of a class 2 transposon is repaired by the host machinery (gap repair). This gap is sometimes repaired by making an identical copy of the excised transposon, using the element still present on the sister chromatid or the homologous chromosome as a template. The process can be incomplete due to slippage and mispairing events. Such aberrant repairs are commonly responsible for the origin of an internally deleted copy of the excised transposon.

PROTOPLAST

A cell after the removal of its cell wall.

BREAKAGE–FUSION–BRIDGE CYCLE

In somatic cells, a cycle of chromosome breakage (at Ds, for example), DNA replication, chromatid fusion (forming a dicentric chromosome) and formation of a chromosome bridge occurs during mitotic anaphase. A new round follows when the chromosome breaks yet again as the two centromeres are pulled to opposite poles.

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Feschotte, C., Jiang, N. & Wessler, S. Plant transposable elements: where genetics meets genomics. Nat Rev Genet 3, 329–341 (2002). https://doi.org/10.1038/nrg793

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