Plant Molecular Biology

, Volume 80, Issue 4–5, pp 419–427 | Cite as

Mobilization of Stowaway-like MITEs in newly formed allohexaploid wheat species

  • Beery Yaakov
  • Khalil Kashkush


Transposable elements (TEs) dominate the genetic capacity of most eukaryotes, especially plants, where they can account for up to 90 % of the genome, such as in wheat. The relationship between TEs and their hosts and the role of TEs in organismal biology are poorly understood. In this study, we have applied next generation sequencing, together with a transposon display technique in order to test whether a Stowaway-like MITE, termed Minos, transposes following allopolyploidization events in wheat. We have generated a 454-pyrosequencing database of Minos-specific amplicons (transposon display products) from a newly formed wheat allohexaploid and its parental lines and retrieved hundreds of novel MITE insertions in the allohexaploid. Clear mobilization of Minos was also seen by site-specific PCR analysis and sequence validation. In addition, using real-time qPCR analysis we observed an insignificant change in the relative quantity of Minos from the expected value of merging the two parental genomes, indicating that, despite its activation, no significant burst in Minos copy number can be seen in the newly formed allohexaploid. Interestingly, we found that CCGG sites surrounding Minos underwent massive hypermethylation following the allohexaploidization process. Our data suggest that MITEs have maintained their capacity for activity throughout the evolution of wheat and might be epigenetically deregulated in the first generations following allopolyploidization.


MITEs Transposable elements DNA methylation Allopolyploidy Wheat 



We would like to thank Moshe Feldman and Hakan Ozkan for providing the seed material. This work was supported by a grant from the Israel Science Foundation (grant # 142/08) to K. K.

Supplementary material

11103_2012_9957_MOESM1_ESM.docx (253 kb)
Supplementary material 1 (DOCX 252 kb)


  1. Baruch O, Kashkush K (2011) Analysis of copy-number variation, insertional polymorphism, and methylation status of the tiniest class I (TRIM) and class II (MITE) transposable element families in various rice strains. Plant Cell Rep 1–9Google Scholar
  2. Beales J, Turner A, GriYths S, Snape JW, Laurie DA (2007) A pseudo-response regulator is misexpressed in the photoperiod insensitive Ppd-D1a mutant of wheat (Triticum aestivum L.). Theor Appl Genet 115:721–733PubMedCrossRefGoogle Scholar
  3. Beaulieu J, Jean M, Belzile F (2009) The allotetraploid Arabidopsis thalianaArabidopsis lyrata subsp petraea as an alternative model system for the study of polyploidy in plants. Mol Genet Genomics 281:421–435PubMedCrossRefGoogle Scholar
  4. Bento M, Pereira HS, Rocheta M, Gustafson P, Viegas W, Silva M (2008) Polyploidization as a retraction force in plant genome evolution: sequence rearrangements in Triticale. PLoS ONE 3:1402–1413CrossRefGoogle Scholar
  5. Blankenberg D, Von Kuster G, Coraor N, Ananda G, Lazarus R, Mangan M, Nekrutenko A, Taylor J (2010) Galaxy: a web-based genome analysis tool for experimentalists. Curr Protoc Mol Biol 19(11–19):10PubMedGoogle Scholar
  6. Brownlie J, Whyard S (2005) Identification of novel non-autonomous CemaT transposable elements and evidence of their mobility within the C. elegans genome. Genetica 125:243–251PubMedCrossRefGoogle Scholar
  7. Bureau TE, Wessler SR (1994a) Mobile inverted-repeat elements of the tourist family are associated with the genes of many cereal grasses. Proc Nat Acad Sci USA 91:1411–1415PubMedCrossRefGoogle Scholar
  8. Bureau TE, Wessler SR (1994b) Stowaway—a new family of inverted repeat elements associated with the genes of both monocotyledonous and dicotyledonous plants. Plant Cell 6:907–916PubMedGoogle Scholar
  9. Chen ZJ (2007) Genetic and epigenetic mechanisms for gene expression and phenotypic variation in plant polyploids. Annu Rev Plant Biol 58:377–406PubMedCrossRefGoogle Scholar
  10. Comai L (2005) The advantages and disadvantages of being polyploid. Nat Rev Genet 6:836–846PubMedCrossRefGoogle Scholar
  11. Feldman M, Levy AA (2005) Allopolyploidy—a shaping force in the evolution of wheat genomes. Cytogenet Genome Res 109:250–258PubMedCrossRefGoogle Scholar
  12. Feldman M, Levy AA (2009) Genome evolution in allopolyploid wheat–a revolutionary reprogramming followed by gradual changes. J Genet Genomics 36:511–518PubMedCrossRefGoogle Scholar
  13. Feschotte C, Pritham EJ (2007) DNA transposons and the evolution of eukaryotic genomes. Annu Rev Genet 41:331–368PubMedCrossRefGoogle Scholar
  14. Feschotte C, Swamy L, Wessler SR (2003) Genome-wide analysis of mariner-like transposable elements in rice reveals complex relationships with Stowaway miniature inverted repeat transposable elements (MITEs). Genetics 163:747–758PubMedGoogle Scholar
  15. Giardine B, Riemer C, Hardison RC, Burhans R, Elnitski L, Shah P, Zhang Y, Blankenberg D, Albert I, Taylor J (2005) Galaxy: a platform for interactive large-scale genome analysis. Genome Res 15:1451–1455PubMedCrossRefGoogle Scholar
  16. Goecks J, Nekrutenko A, Taylor J (2010) Galaxy: a comprehensive approach for supporting accessible, reproducible, and transparent computational research in the life sciences. Genome Biol 11:R86PubMedCrossRefGoogle Scholar
  17. Grandbastien M, Audeon C, Bonnivard E, Casacuberta JM, Chalhoub B, Costa APP, Le QH, Melayah D, Petit M, Poncet C, Tam SM, Van Sluys MA, Mhiri C (2005) Stress activation and genomic impact of Tnt1 retrotransposons in Solanaceae. Cytogenet Genome Res 110:229–241PubMedCrossRefGoogle Scholar
  18. Hikosaka A, Kawahara A (2010) A systematic search and classification of T2 family miniature inverted-repeat transposable elements (MITEs) in Xenopus tropicalis suggests the existence of recently active MITE subfamilies. Mol Genet Genomics 283:49–62PubMedCrossRefGoogle Scholar
  19. Hikosaka A, Nishimura K, Hikosaka-Katayama T, Kawahara A (2011) Recent transposition activity of Xenopus T2 family miniature inverted-repeat transposable elements. Mol Genet Genomics 285:219–224PubMedCrossRefGoogle Scholar
  20. Jiang N, Bao ZR, Zhang XY, Hirochika H, Eddy SR, McCouch SR, Wessler SR (2003) An active DNA transposon family in rice. Nature 421:163–167PubMedCrossRefGoogle Scholar
  21. Jiang N, Feschotte C, Zhang XY, Wessler SR (2004) Using rice to understand the origin and amplification of miniature inverted repeat transposable elements (MITEs). Curr Opin Plant Biol 7:115–119PubMedCrossRefGoogle Scholar
  22. Kashkush K, Khasdan V (2007) Large-scale survey of cytosine methylation of retrotransposons, and the impact of readout transcription from LTRs on expression of adjacent rice genes. Genetics 177:1975–1985PubMedCrossRefGoogle Scholar
  23. Kashkush K, Feldman M, Levy AA (2002) Gene loss, silencing and activation in a newly synthesized wheat allotetraploid. Genetics 160:1651–1659PubMedGoogle Scholar
  24. Kashkush K, Feldman M, Levy AA (2003) Transcriptional activation of retrotransposons alters the expression of adjacent genes in wheat. Nat Genet 33:102–106PubMedCrossRefGoogle Scholar
  25. Khasdan V, Yaakov B, Kraitshtein Z, Kashkush K (2010) Developmental timing of DNA elimination following allopolyploidization in wheat. Genetics 185:387–390PubMedCrossRefGoogle Scholar
  26. Kikuchi K, Terauchi K, Wada M, Hirano HY (2003) The plant MITE mPing is mobilized in anther culture. Nature 421:167–170PubMedCrossRefGoogle Scholar
  27. Kraitshtein Z, Yaakov B, Khasdan V, Kashkush K (2010) Genetic and epigenetic dynamics of a retrotransposon after allopolyploidization of wheat. Genetics 186:801–809PubMedCrossRefGoogle Scholar
  28. Kumar A, Bennetzen JL (1999) Plant retrotransposons. Annu Rev Genet 33:479–532PubMedCrossRefGoogle Scholar
  29. Kumaresan G, Mathavan S (2004) Molecular diversity and phylogenetic analysis of mariner-like transposons in the genome of the silkworm Bombyx mori. Insect Mol Biol 13:259–271PubMedCrossRefGoogle Scholar
  30. Levy AA, Walbot V (1990) Regulation of the timing of transposable element excision during maize development. Science 248:1534–1537PubMedCrossRefGoogle Scholar
  31. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(T)(-Delta Delta C) method. Methods 25:402–408PubMedCrossRefGoogle Scholar
  32. Lukens LN, Pires JC, Leon E, Vogelzang R, Oslach L, Osborn T (2006) Patterns of sequence loss and cytosine methylation within a population of newly resynthesized Brassica napus allopolyploids. Plant Physiol 140:336–348PubMedCrossRefGoogle Scholar
  33. Madlung A, Masuelli RW, Watson B, Reynolds SH, Davison J, Comai L (2002) Remodeling of DNA methylation and phenotypic and transcriptional changes in synthetic Arabidopsis allotetraploids. Plant Physiol 129:733–746PubMedCrossRefGoogle Scholar
  34. Madlung A, Tyagi AP, Watson B, Jiang HM, Kagochi T, Doerge RW, Martienssen R, Comai L (2005) Genomic changes in synthetic Arabidopsis polyploids. Plant J 41:221–230PubMedCrossRefGoogle Scholar
  35. Mansour A (2007) Epigenetic activation of genomic retrotransposons. J Cell Mol Biol 6:99–107Google Scholar
  36. Matzke MA, Matzke AJM (1998) Polyploidy and transposons. Trends Ecol Evol 13:241PubMedCrossRefGoogle Scholar
  37. Miura A, Yonebayashi S, Watanabe K, Toyama T, Shimada H, Kakutani T (2001) Mobilization of transposons by a mutation abolishing full DNA methylation in Arabidopsis. Nature 411:212–214PubMedCrossRefGoogle Scholar
  38. Naito K, Cho E, Yang GJ, Campbell MA, Yano K, Okumoto Y, Tanisaka T, Wessler SR (2006) Dramatic amplification of a rice transposable element during recent domestication. Proc Nat Acad Sci USA 103:17620–17625PubMedCrossRefGoogle Scholar
  39. Naito K, Zhang F, Tsukiyama T, Saito H, Hancock CN, Richardson AO, Okumoto Y, Tanisaka T, Wessler SR (2009) Unexpected consequences of a sudden and massive transposon amplification on rice gene expression. Nature 461:1130–1232PubMedCrossRefGoogle Scholar
  40. Nakazaki T, Okumoto Y, Horibata A, Yamahira S, Teraishi M, Nishida H, Inoue H, Tanisaka T (2003) Mobilization of a transposon in the rice genome. Nature 421:170–172PubMedCrossRefGoogle Scholar
  41. Ngezahayo F, Xu CM, Wang HY, Jiang LL, Pang JS, Liu B (2009) Tissue culture-induced transpositional activity of mPing is correlated with cytosine methylation in rice. BMC Plant Biol 9Google Scholar
  42. Niu B, Fu L, Sun S, Li W (2010) Artificial and natural duplicates in pyrosequencing reads of metagenomic data. BMC Bioinf 11:187CrossRefGoogle Scholar
  43. Ozkan H, Levy AA, Feldman M (2001) Allopolyploidy-Induced rapid genome evolution in the wheat (AegilopsTriticum) group. Plant Cell 13:1735–1747PubMedGoogle Scholar
  44. Parisod C, Salmon A, Zerjal T, Tenaillon M, Grandbastien MA, Ainouche M (2009) Rapid structural and epigenetic reorganization near transposable elements in hybrid and allopolyploid genomes in Spartina. New Phytol 184:1003–1015PubMedCrossRefGoogle Scholar
  45. Parisod C, Alix K, Just J, Petit M, Sarilar V, Mhiri C, Ainouche M, Chalhoub B, Grandbastien MA (2010) Impact of transposable elements on the organization and function of allopolyploid genomes. New Phytol 186:37–45PubMedCrossRefGoogle Scholar
  46. Petit M, Guidat C, Daniel J, Denis E, Montoriol E, Bui QT, Lim KY, Kovarik A, Leitch AR, Grandbastien MA, Mhiri C (2010) Mobilization of retrotransposons in synthetic allotetraploid tobacco. New Phytol 186:135–147PubMedCrossRefGoogle Scholar
  47. Salmon A, Ainouche ML, Wendel JF (2005) Genetic and epigenetic consequences of recent hybridization and polyploidy in Spartina (Poaceae). Mol Ecol 14:1163–1175PubMedCrossRefGoogle Scholar
  48. Sarilar V, Marmagne A, Brabant P, Joets J, Alix K (2011) BraSto, a Stowaway MITE from Brassica: recently active copies preferentially accumulate in the gene space. Plant Mol Biol 77:59–75PubMedCrossRefGoogle Scholar
  49. Shaked H, Kashkush K, Ozkan H, Feldman M, Levy AA (2001) Sequence elimination and cytosine methylation are rapid and reproducible responses of the genome to wide hybridization and allopolyploidy in wheat. Plant Cell 13:1749–1759PubMedGoogle Scholar
  50. Shan X, Liu Z, Dong Z, Wang Y, Chen Y, Lin X, Long L, Han F, Dong Y, Liu B (2005) Mobilization of the active MITE transposons mPing and Pong in rice by introgression from wild rice (Zizania latifolia Griseb.). Mol Biol Evol 22:976–990PubMedCrossRefGoogle Scholar
  51. Shan XH, Ou XF, Liu ZL, Dong YZ, Lin XY, Li XW, Liu B (2009) Transpositional activation of mPing in an asymmetric nuclear somatic cell hybrid of rice and Zizania latifolia was accompanied by massive element loss. Theor Appl Genetics 119:1325–1333CrossRefGoogle Scholar
  52. Wang S, Zhang L, Meyer E, Matz MV (2010) Characterization of a group of MITEs with unusual features from two coral genomes. PLoS ONE 5:e10700PubMedCrossRefGoogle Scholar
  53. Wessler SR (1996) Plant retrotransposons: turned on by stress. Curr Biol 6:959–961PubMedCrossRefGoogle Scholar
  54. Wicker T, Sabot F, Hua-Van A, Bennetzen JL, Capy P, Chalhoub B, Flavell A, Leroy P, Morgante M, Panaud O, Paux E, SanMiguel P, Schulman AH (2007) A unified classification system for eukaryotic transposable elements. Nat Rev Genet 8:973–982PubMedCrossRefGoogle Scholar
  55. Xu YH, Zhong L, Wu XM, Fang XP, Wang JB (2009) Rapid alterations of gene expression and cytosine methylation in newly synthesized Brassica napus allopolyploids. Planta 229:471–483PubMedCrossRefGoogle Scholar
  56. Xu J, Wang M, Zhang X, Tang F, Pan G, Zhou Z (2010) Identification of NbME MITE families: potential molecular markers in the microsporidia Nosema bombycis. J Invertebr Pathol 103:48–52PubMedCrossRefGoogle Scholar
  57. Yaakov B, Kashkush K (2011a) Massive alterations of the methylation patterns around DNA transposons in the first four generations of a newly formed wheat allohexaploid. Genome 54:42–49PubMedCrossRefGoogle Scholar
  58. Yaakov B, Kashkush K (2011b) Methylation, transcription, and rearrangements of transposable elements in synthetic allopolyploids. Int J Plant Genomics. doi: 10.1155/2011/569826
  59. Yaakov B, Ceylan E, Domb K, Kashkush K (2012) Marker utility of miniature inverted-repeat transposable elements for wheat biodiversity and evolution. Theor Appl GenetGoogle Scholar
  60. Yang GJ, Weil CF, Wessler SR (2006) A rice TC1/mariner-like element transposes in yeast. Plant Cell 18:2469–2478PubMedCrossRefGoogle Scholar
  61. Zhao N, Zhu B, Li M, Wang L, Xu L, Zhang H, Zheng S, Qi B, Han F, Liu B (2011) Extensive and heritable epigenetic remodeling and genetic stability accompany allohexaploidization of wheat. Genetics. doi: 10.1534/genetics.111.127688 Google Scholar

Copyright information

© Springer Science+Business Media B.V. 2012

Authors and Affiliations

  1. 1.Department of Life SciencesBen-Gurion UniversityBeer-ShevaIsrael

Personalised recommendations