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Mechanisms of Transposable Element Evolution in Plants and Their Effects on Gene Expression

  • Lisa M. Smith
Chapter

Abstract

Transposable elements are an integral component of plant genomes. Due to their ability to expand or contract in number over relatively short evolutionary periods, the dynamics of transposable elements have a major effect on the evolution of plant genomes. Transposable elements are especially prevalent in pericentromeric regions, although genomic distributions vary according to transposable element family. Transposition-competent transposable elements are generally kept inactive through plant epigenetic mechanisms. These epigenetic control mechanisms mean that regulation of protein-coding gene expression in both euchromatic and heterochromatic regions can result from transposable elements that are proximal to a given gene or integrated into the coding regions or introns. This book chapter examines the dynamics of transposable element evolution and how transposable elements can affect gene expression both directly and indirectly.

Keywords

Transposable elements Epigenetics RNA silencing Gene regulation Natural variation Evolution 

Notes

Acknowledgments

I wish to thank my colleague Dr. Jurriaan Ton of the University of Sheffield for his comments and insightful discussions on the manuscript.

References

  1. 1.
    Lander ES, et al. Initial sequencing and analysis of the human genome. Nature. 2001;409(6822):860–921.PubMedGoogle Scholar
  2. 2.
    Messing J, et al. Sequence composition and genome organization of maize. Proc Natl Acad Sci U S A. 2004;101(40):14349–54.PubMedCentralPubMedGoogle Scholar
  3. 3.
    SanMiguel PJ, et al. Transposable elements, genes and recombination in a 215-kb contig from wheat chromosome 5A(m). Funct Integr Genomics. 2002;2(1–2):70–80.PubMedGoogle Scholar
  4. 4.
    Brenchley R, et al. Analysis of the bread wheat genome using whole-genome shotgun sequencing. Nature. 2012;491(7426):705–10.PubMedCentralPubMedGoogle Scholar
  5. 5.
    Fedoroff NV. Transposable elements, epigenetics, and genome evolution. Science. 2012. 338(6108):758–67.PubMedGoogle Scholar
  6. 6.
    Bennett MD, Leitch IJ. Nuclear DNA amounts in angiosperms: targets, trends and tomorrow. Ann Bot. 2011;107(3):467–590.PubMedCentralPubMedGoogle Scholar
  7. 7.
    Bennetzen JL. Transposable elements, gene creation and genome rearrangement in flowering plants. Curr Opin Genet Dev. 2005;15(6):621–7.PubMedGoogle Scholar
  8. 8.
    SanMiguel P, et al. Nested retrotransposons in the intergenic regions of the maize genome. Science. 1996;274(5288):765–8.PubMedGoogle Scholar
  9. 9.
    Bennetzen JL. Mechanisms and rates of genome expansion and contraction in flowering plants. Genetica. 2002;115(1):29–36.PubMedGoogle Scholar
  10. 10.
    Shirasu K, et al. A contiguous 66-kb barley DNA sequence provides evidence for reversible genome expansion. Genome Res. 2000;10(7):908–15.PubMedCentralPubMedGoogle Scholar
  11. 11.
    Kelly LJ, Leitch IJ. Exploring giant plant genomes with next-generation sequencing technology. Chromosome Res. 2011;19(7):939–53.PubMedGoogle Scholar
  12. 12.
    Ambrozova K, et al. Diverse retrotransposon families and an AT-rich satellite DNA revealed in giant genomes of Fritillaria lilies. Ann Bot. 2011;107(2):255–68.PubMedCentralPubMedGoogle Scholar
  13. 13.
    Ibarra-Laclette E, et al. Architecture and evolution of a minute plant genome. Nature. 2013;498(7452):94–8.PubMedGoogle Scholar
  14. 14.
    Oliver KR, McComb JA, Greene WK. Transposable elements: powerful contributors to angiosperm evolution and diversity. Genome Biol Evol. 2013;5(10):1886–901.PubMedCentralPubMedGoogle Scholar
  15. 15.
    Kapitonov VV, Jurka J. Rolling-circle transposons in eukaryotes. Proc Natl Acad Sci U S A. 2001;98(15):8714–9.PubMedCentralPubMedGoogle Scholar
  16. 16.
    Vitte C, Bennetzen JL. Analysis of retrotransposon structural diversity uncovers properties and propensities in angiosperm genome evolution. Proc Natl Acad Sci U S A. 2006;103(47):17638–43.PubMedCentralPubMedGoogle Scholar
  17. 17.
    Du J, et al. Evolutionary conservation, diversity and specificity of LTR-retrotransposons in flowering plants: insights from genome-wide analysis and multi-specific comparison. Plant J. 2010;63(4):584–98.PubMedGoogle Scholar
  18. 18.
    Casacuberta JM, Santiago N. Plant LTR-retrotransposons and MITEs: control of transposition and impact on the evolution of plant genes and genomes. Gene. 2003;311:1–11.PubMedGoogle Scholar
  19. 19.
    Deragon JM, Casacuberta JM, Panaud O. Plant transposable elements. In: Volff J-N, editor. Plant genomes. Basel: Karger; 2008. p. 69–82.Google Scholar
  20. 20.
    Baucom RS, et al. Exceptional diversity, non-random distribution, and rapid evolution of retroelements in the B73 maize genome. PLoS Genet. 2009;5(11):e1000732.PubMedCentralPubMedGoogle Scholar
  21. 21.
    Bucher E, Reinders J, Mirouze M. Epigenetic control of transposon transcription and mobility in Arabidopsis. Curr Opin Plant Biol. 2012;15(5):503–10.PubMedGoogle Scholar
  22. 22.
    Hollister JD, et al. Transposable elements and small RNAs contribute to gene expression divergence between Arabidopsis thaliana and Arabidopsis lyrata. Proc Natl Acad Sci U S A. 2011;108(6):2322–7.PubMedCentralPubMedGoogle Scholar
  23. 23.
    Jiang N, et al. Pack-MULE transposable elements mediate gene evolution in plants. Nature. 2004;431(7008):569–73.PubMedGoogle Scholar
  24. 24.
    Jia Y, et al. Loss of RNA-dependent RNA polymerase 2 (RDR2) function causes widespread and unexpected changes in the expression of transposons, genes, and 24-nt small RNAs. PLoS Genet. 2009;5(11):e1000737.PubMedCentralPubMedGoogle Scholar
  25. 25.
    Vicient CM. Transcriptional activity of transposable elements in maize. BMC Genomics. 2010;11:601.PubMedCentralPubMedGoogle Scholar
  26. 26.
    Mosher R, et al. Uniparental expression of PolIV-dependent siRNAs in developing endosperm of Arabidopsis. Nature. 2009;460(7252):283–6.PubMedGoogle Scholar
  27. 27.
    Slotkin R, et al. Epigenetic reprogramming and small RNA silencing of transposable elements in pollen. Cell. 2009;136(3):461–72.PubMedCentralPubMedGoogle Scholar
  28. 28.
    Hsieh TF, et al. Genome-wide demethylation of Arabidopsis endosperm. Science. 2009;324(5933):1451–4.PubMedCentralPubMedGoogle Scholar
  29. 29.
    Hu TT, et al. The Arabidopsis lyrata genome sequence and the basis of rapid genome size change. Nat Genet. 2011;43(5):476–81.PubMedCentralPubMedGoogle Scholar
  30. 30.
    Tenaillon MI, et al. Genome size and transposable element content as determined by high-throughput sequencing in maize and Zea luxurians. Genome Biol Evol. 2011;3:219–29.PubMedCentralPubMedGoogle Scholar
  31. 31.
    Hawkins JS, et al. Differential lineage-specific amplification of transposable elements is responsible for genome size variation in Gossypium. Genome Res. 2006;16(10):1252–61.PubMedCentralPubMedGoogle Scholar
  32. 32.
    Piegu B, et al. Doubling genome size without polyploidization: dynamics of retrotransposition-driven genomic expansions in Oryza australiensis, a wild relative of rice. Genome Res. 2006;16(10):1262–9.PubMedCentralPubMedGoogle Scholar
  33. 33.
    Vitte C, Panaud O. LTR retrotransposons and flowering plant genome size: emergence of the increase/decrease model. Cytogenet Genome Res. 2005;110(1–4):91–107.PubMedGoogle Scholar
  34. 34.
    Wang X, Weigel D, Smith LM. Transposon variants and their effects on gene expression in Arabidopsis. PLoS Genet. 2013;9(2):e1003255.PubMedCentralPubMedGoogle Scholar
  35. 35.
    Hollister JD, Gaut BS. Epigenetic silencing of transposable elements: a trade-off between reduced transposition and deleterious effects on neighboring gene expression. Genome Res. 2009;19:1419–28.PubMedCentralPubMedGoogle Scholar
  36. 36.
    Perez-Hormaeche J, et al. Invasion of the Arabidopsis genome by the tobacco retrotransposon Tnt1 is controlled by reversible transcriptional gene silencing. Plant Physiol. 2008;147(3):1264–78.PubMedCentralPubMedGoogle Scholar
  37. 37.
    Mari-Ordonez A, et al. Reconstructing de novo silencing of an active plant retrotransposon. Nat Genet. 2013;45(9):1029–39.PubMedGoogle Scholar
  38. 38.
    Lippman Z, et al. Distinct mechanisms determine transposon inheritance and methylation via small interfering RNA and histone modification. PLoS Biol. 2003;1(3):420–8.Google Scholar
  39. 39.
    Cao X, et al. Role of the DRM and CMT3 methyltransferases in RNA-directed DNA methylation. Curr Biol. 2003;13(24):2212–7.PubMedGoogle Scholar
  40. 40.
    Lippman Z, et al. Role of transposable elements in heterochromatin and epigenetic control. Nature. 2004;430:471–6.PubMedGoogle Scholar
  41. 41.
    Lister R, et al. Highly integrated single-base resolution maps of the epigenome in Arabidopsis. Cell. 2008;133(3):523–36.PubMedCentralPubMedGoogle Scholar
  42. 42.
    Matzke MA, Mette MF, Matzke AJM. Transgene silencing by the host genome defense: implications for the evolution of epigenetic control mechanisms in plants and vertebrates. Plant Mol Biol. 2000;43(2):401–15.PubMedGoogle Scholar
  43. 43.
    Zilberman D, et al. Genome-wide analysis of Arabidopsis thaliana DNA methylation uncovers an interdependence between methylation and transcription. Nat Genet. 2007;39(1):61–9.PubMedGoogle Scholar
  44. 44.
    Kasschau KD, et al. Genome-wide profiling and analysis of Arabidopsis siRNAs. PLoS Biol. 2007;5(3):e57.PubMedCentralPubMedGoogle Scholar
  45. 45.
    Singer T, Yordan C, Martienssen RA. Robertson’s mutator transposons in A. thaliana are regulated by the chromatin-remodeling gene decrease in DNA methylation (DDM1). Genes Dev. 2001;15(5):591–602.PubMedCentralPubMedGoogle Scholar
  46. 46.
    Miura A, et al. Mobilization of transposons by a mutation abolishing full DNA methylation in Arabidopsis. Nature. 2001;411(6834):212–4.PubMedGoogle Scholar
  47. 47.
    Kato M, et al. Role of CG and non-CG methylation in immobilization of transposons in Arabidopsis. Curr Biol. 2003;13(5):421–6.PubMedGoogle Scholar
  48. 48.
    Xie Z, et al. Genetic and functional diversification of small RNA pathways in plants. PLoS Biol. 2004;2(5):642–52.Google Scholar
  49. 49.
    Zilberman D, et al. Role of Arabidopsis ARGONAUTE4 in RNA-directed DNA methylation triggered by inverted repeats. Curr Biol. 2004;14:1214–20.PubMedGoogle Scholar
  50. 50.
    Slotkin RK, Freeling M, Lisch D. Mu killer causes the heritable inactivation of the mutator family of transposable elements in Zea mays. Genetics. 2003;165(2):781–97.PubMedCentralPubMedGoogle Scholar
  51. 51.
    Singh J, Freeling M, Lisch D. A position effect on the heritability of epigenetic silencing. PLoS Genet. 2008;4(10):e1000216.PubMedCentralPubMedGoogle Scholar
  52. 52.
    Wierzbicki AT, Haag JR, Pikaard CS. Noncoding transcription by RNA polymerase Pol IVb/Pol V mediates transcriptional silencing of overlapping and adjacent genes. Cell. 2008;135(4):635–48.PubMedCentralPubMedGoogle Scholar
  53. 53.
    Herr AJ, et al. RNA polymerase IV directs silencing of endogenous DNA. Science. 2005;308(5718):118–20.PubMedGoogle Scholar
  54. 54.
    Onodera Y, et al. Plant nuclear RNA polymerase IV mediates siRNA and DNA methylation-dependent heterochromatin formation. Cell. 2005;120(5):613–22.PubMedGoogle Scholar
  55. 55.
    Gasciolli V, et al. Partially redundant functions of Arabidopsis DICER-like enzymes and a role for DCL4 in producing trans-acting siRNAs. Curr Biol. 2005;15(16):1494–500.PubMedGoogle Scholar
  56. 56.
    Yu B, et al. Methylation as a crucial step in plant microRNA biogenesis. Science. 2005;307:932–5.PubMedGoogle Scholar
  57. 57.
    Li J, et al. Methylation protects miRNAs and siRNAs from a 3’-End uridylation activity in Arabidopsis. Curr Biol. 2005;15:1501–7.PubMedGoogle Scholar
  58. 58.
    Yang Z, et al. HEN1 recognizes 21–24 nt small RNA duplexes and deposits a methyl group onto the 2’ OH of the 3’ terminal nucleotide. Nucleic Acids Res. 2006. 34(2):667–75.PubMedCentralPubMedGoogle Scholar
  59. 59.
    Khvorova A, Reynolds A, Jayasena SD. Functional siRNAs and miRNAs exhibit strand bias. Cell. 2003;115:209–16.PubMedGoogle Scholar
  60. 60.
    Schwarz DS, et al. Asymmetry in the assembly of the RNAi enzyme complex. Cell. 2003;115:199–208.PubMedGoogle Scholar
  61. 61.
    Pontier D, et al. Reinforcement of silencing at transposons and highly repeated sequences requires the concerted action of two distinct RNA polymerases IV in Arabidopsis. Genes Dev. 2005;19:2030–40.PubMedCentralPubMedGoogle Scholar
  62. 62.
    Wierzbicki AT, et al. Spatial and functional relationships among Pol V-associated loci, Pol IV-dependent siRNAs, and cytosine methylation in the Arabidopsis epigenome. Genes Dev. 2012;26(16):1825–36.PubMedCentralPubMedGoogle Scholar
  63. 63.
    Huettel B, et al. Endogenous targets of RNA-directed DNA methylation and Pol IV in Arabidopsis. EMBO J. 2006;25:2828–36.PubMedCentralPubMedGoogle Scholar
  64. 64.
    Li CF, et al. An ARGONAUTE4-containing nuclear processing center colocalized with Cajal bodies in Arabidopsis thaliana. Cell. 2006;126:93–106.PubMedGoogle Scholar
  65. 65.
    Pontes O, et al. The Arabidopsis chromatin-modifying nuclear siRNA pathway involves a nucleolar RNA processing center. Cell. 2006;126:79–92.PubMedGoogle Scholar
  66. 66.
    Law JA, Jacobsen SE. Establishing, maintaining and modifying DNA methylation patterns in plants and animals. Nat Rev Genet. 2010;11(3):204–20.PubMedCentralPubMedGoogle Scholar
  67. 67.
    Aufsatz W, et al. The role of MET1 in RNA-directed de novo and maintenance methylation of CG dinucleotides. Plant Mol Biol. 2004;54(6):793–804.PubMedGoogle Scholar
  68. 68.
    Bartee L, Malagnac F, Bender J. Arabidopsis cmt3 chromomethylase mutations block non-CG methylation and silencing of an endogenous gene. Genes Dev. 2001;15:1753–8.PubMedCentralPubMedGoogle Scholar
  69. 69.
    Ebbs ML, Bartee L, Bender J. H3 lysine 9 methylation is maintained on a transcribed inverted repeat by combined action of SUVH6 and SUVH4 methyltransferases. Mol Cell Biol. 2005;25(23):10507–15.PubMedCentralPubMedGoogle Scholar
  70. 70.
    Ebbs ML, Bender J. Locus-specific control of DNA methylation by the Arabidopsis SUVH5 histone methyltransferase. Plant Cell. 2006;18(5):1166–76.PubMedCentralPubMedGoogle Scholar
  71. 71.
    Jackson JP, et al. Control of CpNpG DNA methylation by the KRYPTONITE histone H3 methyltransferase. Nature. 2002;416(6880):556–60.PubMedGoogle Scholar
  72. 72.
    Malagnac F, Bartee L, Bender J. An Arabidopsis SET domain protein required for maintenance but not establishment of DNA methylation. EMBO J. 2002;21(24):6842–52.PubMedCentralPubMedGoogle Scholar
  73. 73.
    Penterman J, et al. DNA demethylation in the Arabidopsis genome. Proc Natl Acad Sci U S A. 2007;104(16):6752–7.PubMedCentralPubMedGoogle Scholar
  74. 74.
    Rodrigues JA, et al. Imprinted expression of genes and small RNA is associated with localized hypomethylation of the maternal genome in rice endosperm. Proc Natl Acad Sci U S A. 2013;110(19):7934–9.PubMedCentralPubMedGoogle Scholar
  75. 75.
    Ahmed I, et al. Genome-wide evidence for local DNA methylation spreading from small RNA-targeted sequences in Arabidopsis. Nucleic Acids Res. 2011;39(16):6919–31.PubMedCentralPubMedGoogle Scholar
  76. 76.
    Zhang X, et al. Genome-wide high-resolution mapping and functional analysis of DNA methylation in Arabidopsis. Cell. 2006;126(6):1189–201.PubMedGoogle Scholar
  77. 77.
    Cui H, Fedoroff NV. Inducible DNA demethylation mediated by the maize suppressor-mutator transposon-encoded TnpA protein. Plant Cell. 2002;14(11):2883–99.PubMedCentralPubMedGoogle Scholar
  78. 78.
    Feng S, Jacobsen SE. Epigenetic modifications in plants: an evolutionary perspective. Curr Opin Plant Biol. 2011;14(2):179–86.PubMedCentralPubMedGoogle Scholar
  79. 79.
    Zhang X, et al. Genome-wide analysis of mono-, di- and trimethylation of histone H3 lysine 4 in Arabidopsis thaliana. Genome Biol. 2009;10(6):R62.PubMedCentralPubMedGoogle Scholar
  80. 80.
    Zhang X, et al. Whole-genome analysis of histone H3 lysine 27 trimethylation in Arabidopsis. PLoS Biol. 2007;5(5):e129.PubMedCentralPubMedGoogle Scholar
  81. 81.
    Tran RK, et al. Chromatin and siRNA pathways cooperate to maintain DNA methylation of small transposable elements in Arabidopsis. Genome Biol. 2005;6:R90. doi:10.1186/gb-2005–6-11-r90.PubMedCentralPubMedGoogle Scholar
  82. 82.
    Blumenstiel JP. Evolutionary dynamics of transposable elements in a small RNA world. Trends Genet. 2011;27(1):23–31.PubMedGoogle Scholar
  83. 83.
    Gaut BS, et al. Recombination: an underappreciated factor in the evolution of plant genomes. Nat Rev Genet. 2007;8(1):77–84.PubMedGoogle Scholar
  84. 84.
    Bennetzen JL. Transposable element contributions to plant gene and genome evolution. Plant Mol Biol. 2000;42(1):251–69.PubMedGoogle Scholar
  85. 85.
    He F, et al. Widespread interspecific divergence in cis-regulation of transposable elements in the Arabidopsis genus. Mol Biol Evol. 2012;29(3):1081–91.PubMedGoogle Scholar
  86. 86.
    Jin YK, Bennetzen JL. Structure and coding properties of Bs1, a maize retrovirus-like transposon. Proc Natl Acad Sci U S A. 1989;86(16):6235–9.PubMedCentralPubMedGoogle Scholar
  87. 87.
    Johns MA, et al. An unusually compact retrotransposon in maize. Plant Mol Biol. 1989;12(6):633–42.PubMedGoogle Scholar
  88. 88.
    Grandbastien MA, Spielmann A, Caboche M. Tnt1, a mobile retroviral-like transposable element of tobacco isolated by plant cell genetics. Nature. 1989;337(6205):376–80.PubMedGoogle Scholar
  89. 89.
    Pelissier T, et al. Athila, a new retroelement from Arabidopsis thaliana. Plant Mol Biol. 1995;29(3):441–52.PubMedGoogle Scholar
  90. 90.
    Pereira V. Insertion bias and purifying selection of retrotransposons in the Arabidopsis thaliana genome. Genome Biol. 2004;5:R79. doi: 10.1186/gb-2004–5-10-r79.PubMedCentralPubMedGoogle Scholar
  91. 91.
    Frank MJ, et al. Tag1 is an autonomous transposable element that shows somatic excision in both Arabidopsis and tobacco. Plant Cell. 1997;9(10):1745–56.PubMedCentralPubMedGoogle Scholar
  92. 92.
    Tsay YF, et al. Identification of a mobile endogenous transposon in Arabidopsis thaliana. Science. 1993;260(5106):342–4.PubMedGoogle Scholar
  93. 93.
    Lenoir A, et al. The evolutionary origin and genomic organization of SINEs in Arabidopsis thaliana. Mol Biol Evol. 2001;18(12):2315–22.PubMedGoogle Scholar
  94. 94.
    Casacuberta E, Pardue ML. Transposon telomeres are widely distributed in the Drosophila genus: TART elements in the virilis group. Proc Natl Acad Sci U S A. 2003;100(6):3363–8.PubMedCentralPubMedGoogle Scholar
  95. 95.
    Ito H, et al. An siRNA pathway prevents transgenerational retrotransposition in plants subjected to stress. Nature. 2011;472(7341):115–9.PubMedGoogle Scholar
  96. 96.
    Naito K, et al. Dramatic amplification of a rice transposable element during recent domestication. Proc Natl Acad Sci U S A. 2006;103(47):17620–5.PubMedCentralPubMedGoogle Scholar
  97. 97.
    Li Y, Harris L, Dooner HK. TED, an autonomous and rare maize transposon of the mutator superfamily with a high gametophytic excision frequency. Plant Cell. 2013;25(9):3251–65.PubMedCentralPubMedGoogle Scholar
  98. 98.
    Le Rouzic A, Capy P. Population genetics models of competition between transposable element subfamilies. Genetics. 2006;174(2):785–93.PubMedGoogle Scholar
  99. 99.
    Le Rouzic A, Boutin TS, Capy P. Long-term evolution of transposable elements. Proc Natl Acad Sci U S A. 2007;104(49):19375–80.PubMedCentralPubMedGoogle Scholar
  100. 100.
    Rangwala SH, Richards EJ. Differential epigenetic regulation within an Arabidopsis retroposon family. Genetics. 2007;176(1):151–60.PubMedCentralPubMedGoogle Scholar
  101. 101.
    Hamilton AJ, et al. Two classes of short interfering RNA in RNA silencing. EMBO J. 2002;21(17):4671–9.PubMedCentralPubMedGoogle Scholar
  102. 102.
    Zilberman D, Cao X, Jacobsen SE. ARGONAUTE4 control of locus specific siRNA accumulation and DNA and histone methylation. Science. 2003;299:716–9.PubMedGoogle Scholar
  103. 103.
    Mirouze M, et al. Selective epigenetic control of retrotransposition in Arabidopsis. Nature. 2009;461(7262):427–30.PubMedGoogle Scholar
  104. 104.
    Naito K, et al. Unexpected consequences of a sudden and massive transposon amplification on rice gene expression. Nature. 2009;461(7267):1130–4.PubMedGoogle Scholar
  105. 105.
    Huang X, et al. Genome-wide analysis of transposon insertion polymorphisms reveals intraspecific variation in cultivated rice. Plant Physiol. 2008;148(1):25–40.PubMedCentralPubMedGoogle Scholar
  106. 106.
    Warnefors M, Pereira V, Eyre-Walker A. Transposable elements: insertion pattern and impact on gene expression evolution in hominids. Mol Biol Evol. 2010;27(8):1955–62.PubMedGoogle Scholar
  107. 107.
    Fukai E, et al. Derepression of the plant chromovirus LORE1 induces germline transposition in regenerated plants. PLoS Genet. 2010;6(3):e1000868.PubMedCentralPubMedGoogle Scholar
  108. 108.
    Bureau TE, Wessler SR. Tourist: a large family of small inverted repeat elements frequently associated with maize genes. Plant Cell. 1992;4(10):1283–94.PubMedCentralPubMedGoogle Scholar
  109. 109.
    Bureau TE, Ronald PC, Wessler SR. 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;93(16):8524–9.PubMedCentralPubMedGoogle Scholar
  110. 110.
    Wei F, et al. Detailed analysis of a contiguous 22-Mb region of the maize genome. PLoS Genet. 2009;5(11):e1000728.PubMedCentralPubMedGoogle Scholar
  111. 111.
    Zerjal T, et al. Contrasting evolutionary patterns and target specificities among three Tourist-like MITE families in the maize genome. Plant Mol Biol. 2009;71(1–2):99–114.PubMedGoogle Scholar
  112. 112.
    Pan X, Li Y, Stein L. Site preferences of insertional mutagenesis agents in Arabidopsis. Plant Physiol. 2005;137(1):168–75.PubMedCentralPubMedGoogle Scholar
  113. 113.
    Sarilar V, et al. BraSto, a Stowaway MITE from Brassica: recently active copies preferentially accumulate in the gene space. Plant Mol Biol. 2011;77(1–2):59–75.PubMedGoogle Scholar
  114. 114.
    Miyao A, et al. Target site specificity of the Tos17 retrotransposon shows a preference for insertion within genes and against insertion in retrotransposon-rich regions of the genome. Plant Cell. 2003;15(8):1771–80.PubMedCentralPubMedGoogle Scholar
  115. 115.
    Piffanelli P, et al. Large-scale characterization of Tos17 insertion sites in a rice T-DNA mutant library. Plant Mol Biol. 2007;65(5):587–601.PubMedGoogle Scholar
  116. 116.
    Kolesnik T, et al. Establishing an efficient Ac/Ds tagging system in rice: large-scale analysis of Ds flanking sequences. Plant J. 2004;37(2):301–14.PubMedGoogle Scholar
  117. 117.
    Tsukahara S, et al. Centromere-targeted de novo integrations of an LTR retrotransposon of Arabidopsis lyrata. Genes Dev. 2012;26(7):705–13.PubMedCentralPubMedGoogle Scholar
  118. 118.
    Le QH, et al. Transposon diversity in Arabidopsis thaliana. Proc Natl Acad Sci U S A. 2000;97(13):7376–81.PubMedCentralPubMedGoogle Scholar
  119. 119.
    Devos KM, Brown JK, Bennetzen JL. Genome size reduction through illegitimate recombination counteracts genome expansion in Arabidopsis. Genome Res. 2002;12(7):1075–9.PubMedCentralPubMedGoogle Scholar
  120. 120.
    Tian Z, et al. Do genetic recombination and gene density shape the pattern of DNA elimination in rice long terminal repeat retrotransposons? Genome Res. 2009;19(12):2221–30.PubMedCentralPubMedGoogle Scholar
  121. 121.
    Wright SI, Agrawal N, Bureau TE. Effects of recombination rate and gene density on transposable element distributions in Arabidopsis thaliana. Genome Res. 2003;13(8):1897–903.PubMedCentralPubMedGoogle Scholar
  122. 122.
    Buisine N, Quesneville H, Colot V. Improved detection and annotation of transposable elements in sequenced genomes using multiple reference sequence sets. Genomics. 2008;91(5):467–75.PubMedGoogle Scholar
  123. 123.
    Montgomery EA, et al. Chromosome rearrangement by ectopic recombination in Drosophila melanogaster: genome structure and evolution. Genetics. 1991;129(4):1085–98.PubMedCentralPubMedGoogle Scholar
  124. 124.
    Cao J, et al. Whole-genome sequencing of multiple Arabidopsis thaliana populations. Nat Genet. 2011;43(10):956–63.PubMedGoogle Scholar
  125. 125.
    Gan X, et al. Multiple reference genomes and transcriptomes for Arabidopsis thaliana. Nature. 2011;477(7365):419–23.PubMedGoogle Scholar
  126. 126.
    Schneeberger K, et al. Reference-guided assembly of four diverse Arabidopsis thaliana genomes. Proc Natl Acad Sci U S A. 2011;108(25):10249–54.PubMedCentralPubMedGoogle Scholar
  127. 127.
    Hollister JD, Gaut BS. Population and evolutionary dynamics of Helitron transposable elements in Arabidopsis thaliana. Mol Biol Evol. 2007;24(11):2515–24.PubMedGoogle Scholar
  128. 128.
    Ma J, Devos KM, Bennetzen JL. Analyses of LTR-retrotransposon structures reveal recent and rapid genomic DNA loss in rice. Genome Res. 2004;14(5):860–9.PubMedCentralPubMedGoogle Scholar
  129. 129.
    Sabot F, et al. Transpositional landscape of the rice genome revealed by paired-end mapping of high-throughput re-sequencing data. Plant J. 2011;66(2):241–6.PubMedGoogle Scholar
  130. 130.
    Kalendar R, et al. Genome evolution of wild barley (Hordeum spontaneum) by BARE-1 retrotransposon dynamics in response to sharp microclimatic divergence. Proc Natl Acad Sci U S A. 2000;97(12):6603–7.PubMedCentralPubMedGoogle Scholar
  131. 131.
    Ma J, Bennetzen JL. Rapid recent growth and divergence of rice nuclear genomes. Proc Natl Acad Sci U S A. 2004;101(34):12404–10.PubMedCentralPubMedGoogle Scholar
  132. 132.
    Ma J, Bennetzen JL. Recombination, rearrangement, reshuffling, and divergence in a centromeric region of rice. Proc Natl Acad Sci U S A. 2006;103(2):383–8.PubMedCentralPubMedGoogle Scholar
  133. 133.
    Hawkins JS, Grover CE, Wendel JF. Repeated big bangs and the expanding universe: directionality in plant genome size evolution. Plant Sci. 2008;174(6):557–62.Google Scholar
  134. 134.
    Zhang J, Zuo T, Peterson T. Generation of tandem direct duplications by reversed-ends transposition of maize ac elements. PLoS Genet. 2013;9(8):e1003691.PubMedCentralPubMedGoogle Scholar
  135. 135.
    Piriyapongsa J, Jordan IK. Dual coding of siRNAs and miRNAs by plant transposable elements. RNA. 2008;14(5):814–21.PubMedCentralPubMedGoogle Scholar
  136. 136.
    Li Y, et al. Domestication of transposable elements into MicroRNA genes in plants. PLoS One. 2011;6(5):e19212.PubMedCentralPubMedGoogle Scholar
  137. 137.
    Ou-Yang F, et al. Transposable element-associated microRNA hairpins produce 21-nt sRNAs integrated into typical microRNA pathways in rice. Funct Integr Genomics. 2013;13(2):207–16.PubMedCentralPubMedGoogle Scholar
  138. 138.
    Schaack S, Gilbert C, Feschotte C. Promiscuous DNA: horizontal transfer of transposable elements and why it matters for eukaryotic evolution. Trends Ecol Evol. 2010;25(9):537–46.PubMedCentralPubMedGoogle Scholar
  139. 139.
    Cheng X, et al. A new family of Ty1-copia-like retrotransposons originated in the tomato genome by a recent horizontal transfer event. Genetics. 2009;181(4):1183–93.PubMedCentralPubMedGoogle Scholar
  140. 140.
    Diao X, Freeling M, Lisch D. Horizontal transfer of a plant transposon. PLoS Biol. 2006;4(1):e5.PubMedCentralPubMedGoogle Scholar
  141. 141.
    Roulin A, et al. Whole genome surveys of rice, maize and sorghum reveal multiple horizontal transfers of the LTR-retrotransposon Route66 in Poaceae. BMC Evol Biol. 2009;9:58.PubMedCentralPubMedGoogle Scholar
  142. 142.
    Woodrow P, et al. Ty1-copia group retrotransposons and the evolution of retroelements in several angiosperm plants: evidence of horizontal transmission. Bioinformation. 2012;8(6):267–71.PubMedCentralPubMedGoogle Scholar
  143. 143.
    Tenaillon MI, Hollister JD, Gaut BS. A triptych of the evolution of plant transposable elements. Trends Plant Sci. 2010;15(8):471–8.PubMedGoogle Scholar
  144. 144.
    Boutin TS, Le Rouzic A, Capy P. How does selfing affect the dynamics of selfish transposable elements? Mob DNA. 2012;3:5.PubMedCentralPubMedGoogle Scholar
  145. 145.
    Dolgin ES, Charlesworth B. The fate of transposable elements in asexual populations. Genetics. 2006;174(2):817–27.PubMedCentralPubMedGoogle Scholar
  146. 146.
    Wright SI, Schoen DJ. Transposon dynamics and the breeding system. Genetica. 1999;107(1–3):139–48.PubMedGoogle Scholar
  147. 147.
    Agren JA, Wright SI. Co-evolution between transposable elements and their hosts: a major factor in genome size evolution? Chromosome Res. 2011;19(6):777–86.PubMedGoogle Scholar
  148. 148.
    Charlesworth B, Langley CH. The evolution of self-regulated transposition of transposable elements. Genetics. 1986;112(2):359–83.PubMedCentralPubMedGoogle Scholar
  149. 149.
    Yang G, et al. Tuned for transposition: molecular determinants underlying the hyperactivity of a Stowaway MITE. Science. 2009;325(5946):1391–4.PubMedGoogle Scholar
  150. 150.
    de la Chaux N, et al. The predominantly selfing plant Arabidopsis thaliana experienced a recent reduction in transposable element abundance compared to its outcrossing relative Arabidopsis lyrata. Mob DNA. 2012;3(1):2.PubMedCentralPubMedGoogle Scholar
  151. 151.
    Wright SI, et al. Population dynamics of an Ac-like transposable element in self- and cross-pollinating Arabidopsis. Genetics. 2001;158(3):1279–88.PubMedCentralPubMedGoogle Scholar
  152. 152.
    Lockton S, Gaut BS. The evolution of transposable elements in natural populations of self-fertilizing Arabidopsis thaliana and its outcrossing relative Arabidopsis lyrata. BMC Evol Biol. 2010;10:10. doi:10.1186/1471–2148-10–10.PubMedCentralPubMedGoogle Scholar
  153. 153.
    Tam SM, et al. The distribution of copia-type retrotransposons and the evolutionary history of tomato and related wild species. J Evol Biol. 2007;20(3):1056–72.PubMedGoogle Scholar
  154. 154.
    Wright SI, et al. Genomic consequences of outcrossing and selfing in plants. Int J Plant Sci. 2008;169(1):105–118.Google Scholar
  155. 155.
    Charlesworth D, Charlesworth B. Transposable elements in inbreeding and outbreeding populations. Genetics. 1995;140(1):415–7.PubMedCentralPubMedGoogle Scholar
  156. 156.
    Morgan MT. Transposable element number in mixed mating populations. Genet Res. 2001;77(3):261–75.PubMedGoogle Scholar
  157. 157.
    Charlesworth D, Wright SI. Breeding systems and genome evolution. Curr Opin Genet Dev. 2001;11(6):685–90.PubMedGoogle Scholar
  158. 158.
    Matsunaga W, et al. The effects of heat induction and the siRNA biogenesis pathway on the transgenerational transposition of ONSEN, a copia-like retrotransposon in Arabidopsis thaliana. Plant Cell Physiol. 2012;53(5):824–33.PubMedGoogle Scholar
  159. 159.
    Mhiri C. et al. The promoter of the tobacco Tnt1 retrotransposon is induced by wounding and by abiotic stress. Plant Mol Biol. 1997;33(2):257–66.PubMedGoogle Scholar
  160. 160.
    Ivashuta S, et al. Genotype-dependent transcriptional activation of novel repetitive elements during cold acclimation of alfalfa (Medicago sativa). Plant J. 2002;31(5):615–27.PubMedGoogle Scholar
  161. 161.
    Uchiyama T, et al. A pair of transposons coordinately suppresses gene expression, independent of pathways mediated by siRNA in Antirrhinum. New Phytol. 2013;197(2):431–40.PubMedGoogle Scholar
  162. 162.
    Grandbastien MA, et al. Stress activation and genomic impact of Tnt1 retrotransposons in Solanaceae. Cytogenet Genome Res. 2005;110(1–4):229–41.PubMedGoogle Scholar
  163. 163.
    Beguiristain T, et al. Three Tnt1 subfamilies show different stress-associated patterns of expression in tobacco. Consequences for retrotransposon control and evolution in plants. Plant Physiol. 2001;127(1):212–21.PubMedCentralPubMedGoogle Scholar
  164. 164.
    Walbot V. UV-B damage amplified by transposons in maize. Nature. 1999;397(6718):398–9.PubMedGoogle Scholar
  165. 165.
    McClintock B. The significance of responses of the genome to challenge. Science. 1984;226(4676):792–801.PubMedGoogle Scholar
  166. 166.
    Shan X, et al. Mobilization of the active MITE transposons mPing and Pong in rice by introgression from wild rice (Zizania latifolia Griseb.). Mol Biol Evol. 2005;22(4):976–90.PubMedGoogle Scholar
  167. 167.
    Wang N, et al. Transpositional reactivation of the Dart transposon family in rice lines derived from introgressive hybridization with Zizania latifolia. BMC Plant Biol. 2010;10:190.PubMedCentralPubMedGoogle Scholar
  168. 168.
    Zou J, et al. De novo genetic variation associated with retrotransposon activation, genomic rearrangements and trait variation in a recombinant inbred line population of Brassica napus derived from interspecific hybridization with Brassica rapa. Plant J. 2011;68(2):212–24.PubMedGoogle Scholar
  169. 169.
    Kawakami T, et al. Transposable element proliferation and genome expansion are rare in contemporary sunflower hybrid populations despite widespread transcriptional activity of LTR retrotransposons. Genome Biol Evol. 2011;3:156–67.PubMedCentralPubMedGoogle Scholar
  170. 170.
    Wang Q, et al. Intergenomic rearrangements after polyploidization of Kengyilia thoroldiana (Poaceae: Triticeae) affected by environmental factors. PLoS One. 2012;7(2):e31033.PubMedCentralPubMedGoogle Scholar
  171. 171.
    Matzke MA, Matzke AJ. Polyploidy and transposons. Trends Ecol Evol. 1998;13(6):241.PubMedGoogle Scholar
  172. 172.
    Ungerer MC, Strakosh SC, Zhen Y. Genome expansion in three hybrid sunflower species is associated with retrotransposon proliferation. Curr Biol. 2006;16(20):R872–3.PubMedGoogle Scholar
  173. 173.
    Baumel A, et al. Retrotransposons and genomic stability in populations of the young allopolyploid species Spartina anglica C.E. Hubbard (Poaceae). Mol Biol Evol. 2002;19(8):1218–27.PubMedGoogle Scholar
  174. 174.
    Josefsson C, Dilkes B, Comai L. Parent-dependent loss of gene silencing during interspecies hybridization. Curr Biol. 2006;16(13):1322–1328.PubMedGoogle Scholar
  175. 175.
    Burkart-Waco D, et al. Early disruption of maternal-zygotic interaction and activation of defense-like responses in Arabidopsis interspecific crosses. Plant Cell. 2013;25(6):2037–55.PubMedCentralPubMedGoogle Scholar
  176. 176.
    Madlung A, et al. Genomic changes in synthetic Arabidopsis polyploids. Plant J. 2005;41(2):221–30.PubMedGoogle Scholar
  177. 177.
    Kashkush K, Feldman M, Levy AA. Transcriptional activation of retrotransposons alters the expression of adjacent genes in wheat. Nat Genet. 2003;33(1):102–6.PubMedGoogle Scholar
  178. 178.
    Kashkush K, Feldman M, Levy AA. Gene loss, silencing and activation in a newly synthesized wheat allotetraploid. Genetics. 2002;160(4):1651–9.PubMedCentralPubMedGoogle Scholar
  179. 179.
    Parisod C, et al. Rapid structural and epigenetic reorganization near transposable elements in hybrid and allopolyploid genomes in Spartina. New Phytol. 2009;184(4):1003–15.PubMedGoogle Scholar
  180. 180.
    Renny-Byfield S, et al. Next generation sequencing reveals genome downsizing in allotetraploid Nicotiana tabacum, predominantly through the elimination of paternally derived repetitive DNAs. Mol Biol Evol. 2011;28(10):2843–54.PubMedGoogle Scholar
  181. 181.
    Lynch M, Conery JS. The origins of genome complexity. Science. 2003;302(5649):1401–4.PubMedGoogle Scholar
  182. 182.
    Lockton S, Ross-Ibarra J, Gaut BS. Demography and weak selection drive patterns of transposable element diversity in natural populations of Arabidopsis lyrata. Proc Natl Acad Sci U S A. 2008;105(37):13965–70.PubMedCentralPubMedGoogle Scholar
  183. 183.
    Whitney KD, et al. A role for nonadaptive processes in plant genome size evolution? Evolution. 2010;64(7):2097–109.PubMedGoogle Scholar
  184. 184.
    Nystedt B, et al. The Norway spruce genome sequence and conifer genome evolution. Nature. 2013;497(7451):579–84.PubMedGoogle Scholar
  185. 185.
    Bhattacharyya MK, et al. The wrinkled-seed character of pea described by Mendel is caused by a transposon-like insertion in a gene encoding starch-branching enzyme. Cell. 1990;60(1):115–22.PubMedGoogle Scholar
  186. 186.
    Greene B, Walko R, Hake S. Mutator insertions in an intron of the maize knotted1 gene result in dominant suppressible mutations. Genetics. 1994;138(4):1275–85.PubMedCentralPubMedGoogle Scholar
  187. 187.
    Momose M, Abe Y, Ozeki Y. Miniature inverted-repeat transposable elements of Stowaway are active in potato. Genetics. 2010;186(1):59–66.PubMedCentralPubMedGoogle Scholar
  188. 188.
    Scott L, LaFoe D, Weil CF. Adjacent sequences influence DNA repair accompanying transposon excision in maize. Genetics. 1996;142(1):237–46.PubMedCentralPubMedGoogle Scholar
  189. 189.
    Sakai H, Tanaka T, Itoh T. Birth and death of genes promoted by transposable elements in Oryza sativa. Gene. 2007;392(1–2):59–63.PubMedGoogle Scholar
  190. 190.
    Lockton S, Gaut BS. The contribution of transposable elements to expressed coding sequence in Arabidopsis thaliana. J Mol Evol. 2009;68(1):80–9.PubMedGoogle Scholar
  191. 191.
    Chan SW, et al. RNA silencing genes control de novo DNA methylation. Science. 2004;303(5662):1336.PubMedGoogle Scholar
  192. 192.
    Cowan RK, et al. MUSTANG is a novel family of domesticated transposase genes found in diverse angiosperms. Mol Biol Evol. 2005;22(10):2084–9.PubMedGoogle Scholar
  193. 193.
    Joly-Lopez Z, et al. A gene family derived from transposable elements during early angiosperm evolution has reproductive fitness benefits in Arabidopsis thaliana. PLoS Genet. 2012;8(9):e1002931.PubMedCentralPubMedGoogle Scholar
  194. 194.
    Bundock P, Hooykaas P. An Arabidopsis hAT-like transposase is essential for plant development. Nature. 2005;436(7048):282–4.PubMedGoogle Scholar
  195. 195.
    Hudson ME, Lisch DR, Quail PH. The FHY3 and FAR1 genes encode transposase-related proteins involved in regulation of gene expression by the phytochrome A-signaling pathway. Plant J. 2003;34(4):453–71.PubMedGoogle Scholar
  196. 196.
    Tsuchiya T, Eulgem T. An alternative polyadenylation mechanism coopted to the Arabidopsis RPP7 gene through intronic retrotransposon domestication. Proc Natl Acad Sci U S A. 2013;110(37):E3535–43.PubMedCentralPubMedGoogle Scholar
  197. 197.
    Kuang H, et al. Identification of miniature inverted-repeat transposable elements (MITEs) and biogenesis of their siRNAs in the Solanaceae: new functional implications for MITEs. Genome Res. 2009;19(1):42–56.PubMedCentralPubMedGoogle Scholar
  198. 198.
    Sugimoto K, Takeda S, Hirochika H. Transcriptional activation mediated by binding of a plant GATA-type zinc finger protein AGP1 to the AG-motif (AGATCCAA) of the wound-inducible Myb gene NtMyb2. Plant J. 2003;36(4):550–64.PubMedGoogle Scholar
  199. 199.
    Butelli E, et al. Retrotransposons control fruit-specific, cold-dependent accumulation of anthocyanins in blood oranges. Plant Cell. 2012;24(3):1242–55.PubMedCentralPubMedGoogle Scholar
  200. 200.
    Fujii M, et al. Acquisition of aluminium tolerance by modification of a single gene in barley. Nat Commun. 2012;3:713.PubMedCentralPubMedGoogle Scholar
  201. 201.
    Magalhaes JV, et al. A gene in the multidrug and toxic compound extrusion (MATE) family confers aluminum tolerance in sorghum. Nat Genet. 2007;39(9):1156–61.PubMedGoogle Scholar
  202. 202.
    Delhaize E, Ma JF, Ryan PR. Transcriptional regulation of aluminium tolerance genes. Trends Plant Sci. 2012;17(6):341–8.PubMedGoogle Scholar
  203. 203.
    Lister C, Jackson D, Martin C. Transposon-induced inversion in Antirrhinum modifies nivea gene expression to give a novel flower color pattern under the control of cycloidearadialis. Plant Cell. 1993;5(11):1541–53.PubMedCentralPubMedGoogle Scholar
  204. 204.
    Kloeckener-Gruissem B, Vogel JM, Freeling M. The TATA box promoter region of maize Adh1 affects its organ-specific expression. EMBO J. 1992;11(1):157–66.PubMedCentralPubMedGoogle Scholar
  205. 205.
    Kloeckener-Gruissem B, Freeling M. Transposon-induced promoter scrambling: a mechanism for the evolution of new alleles. Proc Natl Acad Sci U S A. 1995;92(6):1836–40.PubMedCentralPubMedGoogle Scholar
  206. 206.
    Hoen DR, Bureau TE. Transposable element exaptation in plants. In: Grandbastien M-A and Casacuberta JM, editors. Plant transposable elements. Springer: Berlin; 2012.Google Scholar
  207. 207.
    Liu J, et al. siRNAs targeting an intronic transposon in the regulation of natural flowering behavior in Arabidopsis. Genes Dev. 2004;18(23):2873–8.PubMedCentralPubMedGoogle Scholar
  208. 208.
    Zerjal T, et al. Maize genetic diversity and association mapping using transposable element insertion polymorphisms. Theor Appl Genet. 2012;124(8):1521–37.PubMedGoogle Scholar
  209. 209.
    Zabala G, Vodkin LO. The wp mutation of glycine max carries a gene-fragment-rich transposon of the CACTA superfamily. Plant Cell. 2005;17(10):2619–32.PubMedCentralPubMedGoogle Scholar
  210. 210.
    Morgante M, et al. Gene duplication and exon shuffling by helitron-like transposons generate intraspecies diversity in maize. Nat Genet. 2005;37(9):997–1002.PubMedGoogle Scholar
  211. 211.
    Brunner S, Pea G, Rafalski A. Origins, genetic organization and transcription of a family of non-autonomous helitron elements in maize. Plant J. 2005;43(6):799–810.PubMedGoogle Scholar
  212. 212.
    Lai J, et al. Gene movement by helitron transposons contributes to the haplotype variability of maize. Proc Natl Acad Sci U S A. 2005;102(25):9068–73.PubMedCentralPubMedGoogle Scholar
  213. 213.
    Hanada K, et al. The functional role of pack-MULEs in rice inferred from purifying selection and expression profile. Plant Cell. 2009;21(1):25–38.PubMedCentralPubMedGoogle Scholar
  214. 214.
    Paterson AH, et al. The Sorghum bicolor genome and the diversification of grasses. Nature. 2009;457(7229):551–6.PubMedGoogle Scholar
  215. 215.
    Abrouk M, et al. Grass microRNA gene paleohistory unveils new insights into gene dosage balance in subgenome partitioning after whole-genome duplication. Plant Cell. 2012;24(5):1776–92.PubMedCentralPubMedGoogle Scholar
  216. 216.
    Oliver KR, Greene WK. Transposable elements: powerful facilitators of evolution. Bioessays. 2009;31(7):703–14.PubMedGoogle Scholar
  217. 217.
    Macas J, et al. Hypervariable 3’ UTR region of plant LTR-retrotransposons as a source of novel satellite repeats. Gene. 2009;448(2):198–206.PubMedGoogle Scholar
  218. 218.
    Gong Z, et al. Repeatless and repeat-based centromeres in potato: implications for centromere evolution. Plant Cell. 2012;24(9):3559–74.PubMedCentralPubMedGoogle Scholar
  219. 219.
    Avramova Z, et al. Matrix attachment regions and structural colinearity in the genomes of two grass species. Nucleic Acids Res. 1998;26(3):761–7.PubMedCentralPubMedGoogle Scholar
  220. 220.
    Zhang X, et al. Global analysis of genetic, epigenetic and transcriptional polymorphisms in Arabidopsis thaliana using whole genome tiling arrays. PLoS Genet. 2008;4:e1000032. doi:10.1371/journal.pgen.1000032.PubMedCentralPubMedGoogle Scholar
  221. 221.
    Lu C, et al. Miniature inverted-repeat transposable elements (MITEs) have been accumulated through amplification bursts and play important roles in gene expression and species diversity in Oryza sativa. Mol Biol Evol. 2012;29(3):1005–17.PubMedCentralPubMedGoogle Scholar
  222. 222.
    Yu A, et al. Dynamics and biological relevance of DNA demethylation in Arabidopsis antibacterial defense. Proc Natl Acad Sci U S A. 2013;110(6):2389–94.PubMedCentralPubMedGoogle Scholar
  223. 223.
    Kashkush K, Khasdan V. Large-scale survey of cytosine methylation of retrotransposons and the impact of readout transcription from long terminal repeats on expression of adjacent rice genes. Genetics. 2007;177(4):1975–85.PubMedCentralPubMedGoogle Scholar
  224. 224.
    Eichten SR, et al. Spreading of heterochromatin is limited to specific families of maize retrotransposons. PLoS Genet. 2012;8(12):e1003127.PubMedCentralPubMedGoogle Scholar
  225. 225.
    Saze H, et al. Control of genic DNA methylation by a jmjC domain-containing protein in Arabidopsis thaliana. Science. 2008;319(5862):462–5.PubMedGoogle Scholar
  226. 226.
    Miura A, et al. An Arabidopsis jmjC domain protein protects transcribed genes from DNA methylation at CHG sites. EMBO J. 2009;28(8):1078–86.PubMedCentralPubMedGoogle Scholar
  227. 227.
    Inagaki S, et al. Autocatalytic differentiation of epigenetic modifications within the Arabidopsis genome. EMBO J. 2010;29(20):3496–506.PubMedCentralPubMedGoogle Scholar
  228. 228.
    Saze H, et al. Mechanism for full-length RNA processing of Arabidopsis genes containing intragenic heterochromatin. Nat Commun. 2013;4:2301.PubMedGoogle Scholar
  229. 229.
    McCue AD, et al. Gene expression and stress response mediated by the epigenetic regulation of a transposable element small RNA. PLoS Genet. 2012;8(2):e1002474.PubMedCentralPubMedGoogle Scholar
  230. 230.
    Yan Y, et al. Small RNAs from MITE-derived stem-loop precursors regulate abscisic acid signaling and abiotic stress responses in rice. Plant J. 2011;65(5):820–8.PubMedGoogle Scholar
  231. 231.
    Nosaka M, et al. Role of transposon-derived small RNAs in the interplay between genomes and parasitic DNA in rice. PLoS Genet. 2012;8(9):e1002953.PubMedCentralPubMedGoogle Scholar
  232. 232.
    Schott G, et al. Differential effects of viral silencing suppressors on siRNA and miRNA loading support the existence of two distinct cellular pools of ARGONAUTE1. EMBO J. 2012;31(11):2553–65.PubMedCentralPubMedGoogle Scholar
  233. 233.
    Rabinowicz PD, et al. Genes and transposons are differentially methylated in plants, but not in mammals. Genome Res. 2003;13(12):2658–64.PubMedCentralPubMedGoogle Scholar
  234. 234.
    Vaughn MW, et al. Epigenetic natural variation in Arabidopsis thaliana. PLoS Biol. 2007;5:e174. doi: 10.1371/journal.pbio.0050174.PubMedCentralPubMedGoogle Scholar
  235. 235.
    Cokus SJ, et al. Shotgun bisulphite sequencing of the Arabidopsis genome reveals DNA methylation patterning. Nature. 2008;452(7184):215–9.PubMedCentralPubMedGoogle Scholar
  236. 236.
    Ossowski S, et al. The rate and molecular spectrum of spontaneous mutations in Arabidopsis thaliana. Science. 2010;327(5961):92–4.PubMedGoogle Scholar
  237. 237.
    Lisch D. Epigenetic regulation of transposable elements in plants. Ann Rev Plant Biol. 2009;60:43–66.Google Scholar
  238. 238.
    Mochizuki K, Gorovsky MA. Conjugation-specific small RNAs in Tetrahymena have predicted properties of scan (scn) RNAs involved in genome rearrangement. Genes Dev. 2004;18(17):2068–73.PubMedCentralPubMedGoogle Scholar
  239. 239.
    Mochizuki K, et al. Analysis of a piwi-related gene implicates small RNAs in genome rearrangement in Tetrahymena. Cell. 2002;110(6):689–99.PubMedGoogle Scholar
  240. 240.
    Zhai J, et al. Small RNA-directed epigenetic natural variation in Arabidopsis thaliana. PLoS Genet. 2008;4(4):e1000056.PubMedCentralPubMedGoogle Scholar
  241. 241.
    Groszmann M, et al. Changes in 24-nt siRNA levels in Arabidopsis hybrids suggest an epigenetic contribution to hybrid vigor. Proc Natl Acad Sci USA. 2011;108(6):2617–22.PubMedCentralPubMedGoogle Scholar
  242. 242.
    Zeh DW, Zeh JA, Ishida Y. Transposable elements and an epigenetic basis for punctuated equilibria. Bioessays. 2009;31(7):715–26.PubMedGoogle Scholar

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© Springer Science+Business Media New York 2015

Authors and Affiliations

  1. 1.Department of Animal and Plant SciencesUniversity of SheffieldSheffieldUK

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