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Chromosome Research

, Volume 22, Issue 4, pp 559–571 | Cite as

The diversification and activity of hAT transposons in Musa genomes

  • Gerhard Menzel
  • Tony Heitkam
  • Kathrin M. Seibt
  • Faisal Nouroz
  • Manuela Müller-Stoermer
  • John S. Heslop-Harrison
  • Thomas Schmidt
Article

Abstract

Sequencing of plant genomes often identified the hAT superfamily as the largest group of DNA transposons. Nevertheless, detailed information on the diversity, abundance and chromosomal localization of plant hAT families are rare. By in silico analyses of the reference genome assembly and bacterial artificial chromosome (BAC) sequences, respectively, we performed the classification and molecular characterization of hAT transposon families in Musa acuminata. Musa hAT transposons are organized in three families designated MuhAT I, MuhAT II and MuhAT III. In total, 70 complete autonomous elements of the MuhAT I and MuhAT II families were detected, while no autonomous MuhAT III transposons were found. Based on the terminal inverted repeat (TIR)-specific sequence information of the autonomous transposons, 1722 MuhAT I- and MuhAT II-specific miniature inverted-repeat transposable elements (MuhMITEs) were identified. Autonomous MuhAT I and MuhAT II elements are only moderately abundant in the sections of the genus Musa, while the corresponding MITEs exhibit an amplification in Musa genomes. By fluorescent in situ hybridization (FISH), autonomous MuhAT transposons as well as MuhMITEs were localized in subtelomeric, most likely gene-rich regions of M. acuminata chromosomes. A comparison of homoeologous regions of M. acuminata and Musa balbisiana BACs revealed the species-specific mobility of MuhMITEs. In particular, the activity of MuhMITEs II showing transduplications of genomic sequences might indicate the presence of active MuhAT transposons, thus suggesting a potential role of MuhMITEs as modulators of genome evolution of Musa.

Keywords

Musa acuminata Musa balbisiana Genome assembly BAC hAT transposons FISH 

Notes

Acknowledgments

We are indebted to Nadin Fliegner and Ines Walter for the excellent technical assistance. We thank the DAAD-British Council ARC Academic Research Collaboration project for support of the collaboration. We thank the Centre de Cooperation Internationale en Recherche Agronomique pour le Developpement (CIRAD), Montpellier (France), and the Musa Genome Resource Centre (MGRC) at the Institute of Experimental Botany (IEB), Olomouc (Czech Republic) for the production, storage and distribution of Musa DNA samples used here. We thank the TU Dresden Center for Information Services and High Performance Computing (ZIH) for the computer time allocations.

Conflict of interest

The authors Gerhard Menzel, Tony Heitkam, Kathrin M. Seibt, Faisal Nouroz, Manuela Müller-Stoermer, John S. Heslop-Harrison and Thomas Schmidt declare that they have no conflict of interest.

Supplementary material

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References

  1. Alix K, Heslop-Harrison JS (2004) The diversity of retroelements in diploid and allotetraploid Brassica species. Plant Mol Biol 54:895–909PubMedCrossRefGoogle Scholar
  2. Benjak A, Forneck A, Casacuberta JM (2008) Genome-wide analysis of the “cut-and-paste” transposons of grapevine. PLoS ONE 3:e3107PubMedCentralPubMedCrossRefGoogle Scholar
  3. Benjak A, Boué S, Forneck A, Casacuberta JM (2009) Recent amplification and impact of MITEs on the genome of grapevine (Vitis vinifera L.). Genome Biol Evol 20:75–84Google Scholar
  4. Bennetzen JL (2005) Transposable elements, gene creation and genome rearrangement in flowering plants. Curr Opin Genet Dev 15:621–627PubMedCrossRefGoogle Scholar
  5. Birney E, Clamp M, Durbin R (2004) GeneWise and Genomewise. Genome Res 14:988–995PubMedCentralPubMedCrossRefGoogle Scholar
  6. Capy P, Bazin C, Higuet D, Langin T (1998) Dynamics and evolution of transposable elements. Springer, AustinGoogle Scholar
  7. Cavallini A, Natali L, Zuccolo A, Giordani T, Jurman I, Ferrillo V, Vitacolonna N, Sarri V, Cattonaro F, Ceccarelli M, Cionini PG, Morgante M (2010) Analysis of transposons and repeat composition of the sunflower (Helianthus annuus L.) genome. Theor Appl Genet 120:491–508PubMedCrossRefGoogle Scholar
  8. Chen J, Hu Q, Zhang Y, Lu C, Kuang H (2014) P-MITE: a database for plant miniature inverted-repeat transposable elements. Nucleic Acids Res 42:D1176–D1181PubMedCentralPubMedCrossRefGoogle Scholar
  9. Cheung F, Town CD (2007) A BAC end view of the Musa acuminata genome. BMC Plant Biol 7:29PubMedCentralPubMedCrossRefGoogle Scholar
  10. Crooks GE, Hon G, Chandonia JM, Brenner SE (2004) WebLogo: a sequence logo generator. Genome Res 14:1188–1190PubMedCentralPubMedCrossRefGoogle Scholar
  11. D’Hont A, Denoeud F, Aury JM, Baurens FC, Carreel F, Garsmeur O, Noel B, Bocs S, Droc G, Rouard M, Da Silva C, Jabbari K, Cardi C, Poulain J, Souquet M, Labadie K, Jourda C, Lengellé J, Rodier-Goud M, Alberti A, Bernard M, Correa M, Ayyampalayam S, Mckain MR, Leebens-Mack J, Burgess D, Freeling M, Mbéguié-A-Mbéguié D, Chabannes M, Wicker T, Panaud O, Barbosa J, Hribova E, Heslop-Harrison P, Habas R, Rivallan R, Francois P, Poiron C, Kilian A, Burthia D, Jenny C, Bakry F, Brown S, Guignon V, Kema G, Dita M, Waalwijk C, Joseph S, Dievart A, Jaillon O, Leclercq J, Argout X, Lyons E, Almeida A, Jeridi M, Dolezel J, Roux N, Risterucci AM, Weissenbach J, Ruiz M, Glaszmann JC, Quétier F, Yahiaoui N, Wincker P (2012) The banana (Musa acuminata) genome and the evolution of monocotyledonous plants. Nature 488:213–217PubMedCrossRefGoogle Scholar
  12. Davey MW, Gudimella R, Harikrishna JA, Sin LW, Khalid N, Keulemans W (2013) A draft Musa balbisiana genome sequence for molecular genetics in polyploid, inter- and intra-specific Musa hybrids. BMC Genomics 14:683PubMedCentralPubMedCrossRefGoogle Scholar
  13. de Freitas Ortiz M, Lorenzatto KR, Corrêa BR, Loreto EL (2010) hAT transposable elements and their derivatives: an analysis in the 12 Drosophila genomes. Genetica 138:649–655PubMedCrossRefGoogle Scholar
  14. Desel C (2002) Chromosomale Lokalisierung von repetitiven und unikalen DNA-Sequenzen durch Fluoreszenz- in situ- Hybridisierung in der Genomanalyse bei Beta-Arten. Dissertation, University of KielGoogle Scholar
  15. Droc G, Lariviere D, Guignon V, Yahiaoui N, This D, Garsmeur O, Dereeper A, Hamelin C, Argout X, Dufayard J-F, Lengelle J, Baurens F-C, Cenci A, Pitollat B, D’Hont A, Ruiz M, Rouard M, Bocs S (2013) The Banana Genome Hub. Database. doi: 10.1093/database/bat035 PubMedCentralPubMedGoogle Scholar
  16. Du J, Grant D, Tian Z, Nelson RT, Zhu L, Shoemaker RC, Ma J (2010) SoyTEdb: a comprehensive database of transposable elements in the soybean genome. BMC Genomics 11:113PubMedCentralPubMedCrossRefGoogle Scholar
  17. Eddy SR (1998) Profile hidden Markov models. Bioinformatics 14:755–763PubMedCrossRefGoogle Scholar
  18. Feschotte C, Jiang N, Wessler SR (2002) Plant transposable elements: where genetics meets genomics. Nat Rev Genet 3:329–341PubMedCrossRefGoogle Scholar
  19. 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 163:747–758PubMedCentralPubMedGoogle Scholar
  20. Finnegan DJ (1989) Eukaryotic transposable elements and genome evolution. Trends Genet 5:103–107PubMedCrossRefGoogle Scholar
  21. Fujino K, Sekiguchi H, Kiguchi T (2005) Identification of an active transposon in intact rice plants. Mol Genet Genomics 273:150–157PubMedCrossRefGoogle Scholar
  22. Gambin T, Startek M, Walczak K, Paszek J, Grzebelus D, Gambin A (2013) TIRfinder: a web tool for mining class II transposons carrying terminal inverted repeats. Evol Bioinform Online 9:17–27PubMedCentralCrossRefGoogle Scholar
  23. Häkkinen M (2013) Reappraisal of sectional taxonomy in Musa (Musaceae). Taxon 62:809–813CrossRefGoogle Scholar
  24. Hartings H, Rossi V, Lazzaroni N, Thompson RD, Salamini F, Motto M (1991) Nucleotide sequence of the Bg transposable element of Zea mays L. Maydica 36:355–359Google Scholar
  25. Heslop-Harrison JS, Schwarzacher T (2007) Domestication, genomics and the future for banana. Ann Bot 100:1073–1084PubMedCentralPubMedCrossRefGoogle Scholar
  26. Heslop-Harrison JS, Schwarzacher T (2011) Organisation of the plant genome in chromosomes. Plant J 66:18–33PubMedCrossRefGoogle Scholar
  27. Holligan D, Zhang X, Jiang N, Pritham EJ, Wessler SR (2006) The transposable element landscape of the model legume Lotus japonicus. Genetics 174:2215–2228PubMedCentralPubMedCrossRefGoogle Scholar
  28. Huang J, Zhang K, Shen Y, Huang Z, Li M, Tang D, Gu M, Cheng Z (2009) Identification of a high frequency transposon induced by tissue culture, nDaiZ, a member of the hAT family in rice. Genomics 93:274–281PubMedCrossRefGoogle Scholar
  29. Juretic N, Hoen DR, Huynh ML, Harrison PM, Bureau TE (2005) The evolutionary fate of MULE-mediated duplications of host gene fragments in rice. Genome Res 15:1292–1297PubMedCentralPubMedCrossRefGoogle Scholar
  30. Kuromori T, Hirayama T, Kiyosue Y, Takabe H, Mizukado S, Sakurai T, Akiyama K, Kamiya A, Ito T, Shinozaki K (2004) A collection of 11 800 single-copy Ds transposon insertion lines in Arabidopsis. Plant J 37:897–905PubMedCrossRefGoogle Scholar
  31. Macas J, Koblízková A, Neumann P (2005) Characterization of Stowaway MITEs in pea (Pisum sativum L.) and identification of their potential master elements. Genome 48:831–839PubMedCrossRefGoogle Scholar
  32. Menzel G, Dechyeva D, Keller H, Lange C, Himmelbauer H, Schmidt T (2006) Mobilization and evolutionary history of miniature inverted-repeat transposable elements (MITEs) in Beta vulgaris L. Chromosome Res 14:831–844PubMedCrossRefGoogle Scholar
  33. Menzel G, Krebs C, Diez M, Holtgräwe D, Weisshaar B, Minoche AE, Dohm JC, Himmelbauer H, Schmidt T (2012) Survey of sugar beet (Beta vulgaris L.) hAT transposons and MITE-like hATpin derivatives. Plant Mol Biol 78:393–405PubMedCrossRefGoogle Scholar
  34. Moon S, Jung KH, Lee DE, Jiang WZ, Koh HJ, Heu MH, Lee DS, Suh HS, An G (2006) Identification of active transposon dTok, a member of the hAT family, in rice. Plant Cell Physiol 47:1473–1483PubMedCrossRefGoogle Scholar
  35. Moreno-Vázquez S, Ning J, Meyers BC (2005) hATpin, a family of MITE-like hAT mobile elements conserved in diverse plant species that forms highly stable secondary structures. Plant Mol Biol 58:869–886PubMedCrossRefGoogle Scholar
  36. Novák P, Hřibová E, Neumann P, Koblížková A, Doležel J, Macas J (2014) Genome-wide analysis of repeat diversity across the family Musaceae. PLoS ONE 9:e98918PubMedCentralPubMedCrossRefGoogle Scholar
  37. Rubin E, Lithwick G, Levy AA (2001) Structure and evolution of the hAT transposon superfamily. Genetics 158:949–957PubMedCentralPubMedGoogle Scholar
  38. Saghai-Maroof MA, Soliman KM, Jorgensen RA, Allard RW (1984) Ribosomal DNA spacer-length polymorphisms in barley: mendelian inheritance, chromosomal location, and population dynamics. Proc Natl Acad Sci U S A 81:8014–8018PubMedCentralPubMedCrossRefGoogle Scholar
  39. Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory Press, New YorkGoogle Scholar
  40. Schwarzacher T, Heslop-Harrison JS (2000) Practical in-situ hybridization. BIOS Scientific Publishers, Oxford, p 60Google Scholar
  41. Vollbrecht E, Duvick J, Schares JP, Ahern KR, Deewatthanawong P, Xu L, Conrad LJ, Kikuchi K, Kubinec TA, Hall BD, Weeks R, Unger-Wallace E, Muszynski M, Brendel VP, Brutnell TP (2010) Genome-wide distribution of transposed dissociation elements in maize. Plant Cell 22:1667–1685PubMedCentralPubMedCrossRefGoogle Scholar
  42. 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
  43. Xu Z, Dooner HK (2005) Mx-rMx, a family of interacting transposons in the growing hAT superfamily of maize. Plant Cell 17:375–388PubMedCentralPubMedCrossRefGoogle Scholar
  44. Yang G, Weil CF, Wessler SR (2006) A rice Tc1/mariner-like element transposes in yeast. Plant Cell 18:2469–2478PubMedCentralPubMedCrossRefGoogle Scholar
  45. Zhang X, Wessler SR (2004) Genome-wide comparative analysis of the transposable elements in the related species Arabidopsis thaliana and Brassica oleracea. Proc Natl Acad Sci U S A 101:5589–5594PubMedCentralPubMedCrossRefGoogle Scholar
  46. Zhang X, Jiang N, Feschotte C, Wessler SR (2004) PIF- and Pong-like transposable elements: distribution, evolution and relationship with Tourist-like miniature inverted-repeat transposable elements. Genetics 166:971–986PubMedCentralPubMedCrossRefGoogle Scholar
  47. Zhou L, Mitra R, Atkinson PW, Hickman AB, Dyda F, Craig NL (2004) Transposition of hAT elements links transposable elements and V(D)J recombination. Nature 432:995–1001PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2014

Authors and Affiliations

  • Gerhard Menzel
    • 1
  • Tony Heitkam
    • 1
  • Kathrin M. Seibt
    • 1
  • Faisal Nouroz
    • 2
  • Manuela Müller-Stoermer
    • 1
  • John S. Heslop-Harrison
    • 2
  • Thomas Schmidt
    • 1
  1. 1.Institute of BotanyTechnische Universität DresdenDresdenGermany
  2. 2.Department of BiologyUniversity of LeicesterLeicesterUK

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