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Journal of Molecular Evolution

, Volume 70, Issue 3, pp 275–288 | Cite as

A Helitron-Like Transposon Superfamily from Lepidoptera Disrupts (GAAA)n Microsatellites and is Responsible for Flanking Sequence Similarity within a Microsatellite Family

  • Brad S. CoatesEmail author
  • Douglas V. Sumerford
  • Richard L. Hellmich
  • Leslie C. Lewis
Article

Abstract

Transposable elements (TEs) are mobile DNA regions that alter host genome structure and gene expression. A novel 588 bp non-autonomous high copy number TE in the Ostrinia nubilalis genome has features in common with miniature inverted-repeat transposable elements (MITEs): high A + T content (62.3%), lack of internal protein coding sequence, and secondary structure consisting of subterminal inverted repeats (SIRs). The O. nubilalis TE has inserted at (GAAA)n microsatellite loci, and was named the microsatellite-associated interspersed nuclear element (MINE-1). Non-autonomous MINE-1 superfamily members also were identified downstream of (GAAA)n microsatellites within Bombyx mori and Pectinophora gossypiella genomes. Of 316 (GAAA)n microsatellites from the B. mori whole genome sequence, 201 (63.6%) have associated autonomous or non-autonomous MINE-1 elements. Autonomous B. mori MINE-1s a encode a helicase and endonuclease domain RepHel-like protein (BMHELp1) indicating their classification as Helitron-like transposons and were renamed Helitron1_BM. Transposition of MINE-1 members in Lepidoptera has resulted in the disruption of (GAAA)n microsatellite loci, has impacted the application of microsatellite-based genetic markers, and suggests genome sequence that flanks TT/AA dinucleotides may be required for target site recognition by RepHel endonuclease domains.

Keywords

Microsatellite family Transposable element Mobile element 

Notes

Acknowledgments

This research is a joint contribution from the United States Department of Agriculture Agriculture Research Service and the Iowa Agriculture and Home Economics Experiment Station, Ames (project 3543). Mention of proprietary products does not constitute an endorsement or a recommendation by USDA, or Iowa State University for its use.

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References

  1. Akagi H, Yokozeki Y, Inagaki A, Mori K, Fujimura T (2001) Micron, a microsatellite-targeting transposable element in the rice genome. Mol Genet Genomics 266:471–480CrossRefPubMedGoogle Scholar
  2. Anderson SJ, Gould P, Freeland JR (2007) Repetitive flanking sequences (ReFS): novel molecular markers from microsatellite families. Mol Ecol Notes 7:374–376CrossRefGoogle Scholar
  3. Anthony N, Gelembiuk G, Raterman D, Nice C, Ffrench-Constant R (2001) Brief report: isolation and characterization of microsatellite markers from the endangered Karner blue butterfly Lycaeides melissa samuelis (Lepidoptera). Hereditas 134:271–273CrossRefPubMedGoogle Scholar
  4. Arcot SS, Wang Z, Weber JL, Deininger PL, Batzer MA (1995) Alu repeats: a source for the genesis of primate microsatellites. Genomics 29:136–144CrossRefPubMedGoogle Scholar
  5. Bergman CM, Quesneville H (2007) Discovering and detecting transposable elements in genome sequences. Brief Bioinform 8:382–392CrossRefPubMedGoogle Scholar
  6. Bidichandani SI, Ashizawa T, Patel PI (1998) The GAA triplet-repeat expansion in Friedrich ataxia interferes with transcription and may be associated with an unusual DNA structure. Am J Hum Genet 62:111–121CrossRefPubMedGoogle Scholar
  7. Bork P, Koonin EV (1993) An expanding family of helicase within the ‘DEAD/H’ superfamily. Nucleic Acids Res 11:751–752CrossRefGoogle Scholar
  8. Brunner S, Fengler K, Morgante M, Tingey S, Rafalski A (2005) Evolution of DNA sequence nonhomologies among maize inbreds. Plant Cell 17:343–360CrossRefPubMedGoogle Scholar
  9. Bureau TE, Wessler SR (1994a) Mobile inverted-repeat elements of the Tourist family are associated with the genes of many cereal grasses. Proc Natl Acad Sci USA 91:1411–1415CrossRefPubMedGoogle Scholar
  10. 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 6:907–916CrossRefPubMedGoogle Scholar
  11. Casacuberta E, Casacuberta JM, Puigdomenech P, Monfort A (1998) Presence of miniature inverted-repeat transposable elements (MITEs) in the genome of Arabidopsis thaliana: characterisation of the Emigrant family of elements. Plant J 16:79–85CrossRefPubMedGoogle Scholar
  12. Chen S, Li X (2007) Transposable elements are enriched within or in close proximity to xenobiotic-metabolizing cytochrome P450 genes. BMC Evol Biol 7:46CrossRefPubMedGoogle Scholar
  13. Coates BS, Sumerford DS, Hellmich RL, Lewis LC (2009) Repetitive genome elements in a European corn borer, Ostrinia nubilalis, bacterial artificial chromosome library was indicated by (BAC) end sequencing and development of sequence tag site (STS) markers: Implications for lepidopteran genomic research. Genome (in press)Google Scholar
  14. Craig NL (1995) Unity in transposition reactions. Science 270:253–254CrossRefPubMedGoogle Scholar
  15. Du C, Fefelova N, Caronna J, He L, Dooner HK (2009) The polychromatic Helitron landscape of the maize genome. Proc Natl Acad Sci USA 106:19916–19921PubMedGoogle Scholar
  16. Dufresne M, Hua-Van A, El Wahab HA, Ben M’Barek S, Vasnier C, Teysset L, Kema GHJ, Daboussi MJ (2006) Transposition of a fungal MITE through the action of a Tc1-like transposase. Genetics 175:441–452CrossRefPubMedGoogle Scholar
  17. Economou EP, Bergen AW, Warren AC, Antonarakis SE (1990) The poly(A) tract of Alu repetitive elements is polymorphic in the human genome. Proc Natl Acad Sci USA 87:2951–2954CrossRefPubMedGoogle Scholar
  18. Fauvelot C, Cleary DFR, Menen SBJ (2006) Short-term impact of 1997/1998 ENSO-induced disturbance on abundance and genetic variation in a tropical butterfly. J Heredity 97:367–380CrossRefGoogle Scholar
  19. Feschotte CM, Mouchès C (2000) Evidence that a family of miniature inverted repeat transposable elements (MITEs) from the Arabidopsis thaliana genome has arisen from a pogo-like DNA transpsoson. Mol Biol Evol 17:730–737PubMedGoogle Scholar
  20. Galagan JE, Calvo SE, Cuomo C, Ma LJ, Wortman JR, Batzaglou S, Lee SI, Basturkmen M, Spevak CC, Clutterbuck J, Kapitonov V, Jurka J, Scazzocchio C, Farman M, Butler J, Purcell S, Harris S et al (2005) Sequencing of Aspergillus nidulans and comparative analysis with A. fumigatus and A. oryzae. Nature 438:1105–1115CrossRefPubMedGoogle Scholar
  21. Gupta S, Gallavotti A, Stryker GA, Lai SK (2005) A novel class of Helitron-related transposable elements in maize contain portions of multiple pseudogenes. Plant Mol Biol 57:115–127CrossRefPubMedGoogle Scholar
  22. Hutchison C III, Hardies S, Loeb D, Shehee W, Edgell M (1989) LINEs and related retroposons: long interspersed repeated sequences in the eucaryotic genome. In: Berg DE, Howe MM (eds) Mobile DNA. American Society for Microbiology, Washington, DC, pp 593–617Google Scholar
  23. Jelinek WR, Toomey TP, Leinwand L, Duncan CH, Biro PA, Choudary PV, Weissman SM, Rubin CM, Houck CM, Denlinger PL, Schmid CW (1980) Ubiquitous, interspersed repeated sequences in mammalian genomes. Proc Natl Acad Sci USA 77:1398–1402CrossRefPubMedGoogle Scholar
  24. Jurka J, Pethiyagoda C (1995) Sequences from primates: compilation and analysis. J Mol Evol 40:120–126CrossRefPubMedGoogle Scholar
  25. Kapitonov VV, Jurka J (2001) Rolling-circle transposons in eukaryotes. Proc Natl Acad Sci USA 98:8714–8719CrossRefPubMedGoogle Scholar
  26. Kapitonov VV, Jurka J (2007a) Helitrons in fruit flies. Rephase reports 7:132–271Google Scholar
  27. Kapitonov VV, Jurka J (2007b) Helitrons on a roll: eukaryotic rolling-circle transposons. Trend Genet 23:521–529CrossRefGoogle Scholar
  28. Kofler R, Schlotterer C, Lelley T (2007) SciRoKo: a new tool for whole genome microsatellite search and investigation. Bioinformatics 23:1683–1685CrossRefPubMedGoogle Scholar
  29. Kudo Y, Okazaki S, Anzai T, Fujiwara H (2001) Structural and phylogenetic analysis of TRAS, telomeric repeat-specific non-LTR retrotransposon families in Lepidopteran insects. Mol Biol Evol 18:848–857Google Scholar
  30. Lai J, Li Y, Messing J, Dooner H (2005) Gene movement by Helitron transposons contributes to the haplotype variability in maize. Proc Natl Acad Sci USA 102:9068–9073CrossRefPubMedGoogle Scholar
  31. Lal SK, Hannah L (2005) Helitrons contribute to the lack of gene colinearity observed in modern maize inbreds. Proc Natl Acad Sci USA 102:9993–9994CrossRefPubMedGoogle Scholar
  32. Lerat E, Sémon M (2007) Influence of the transposable element neighborhood on human gene expression in normal and tumor tissues. Gene 396:303–311CrossRefPubMedGoogle Scholar
  33. Levinson G, Gutman GA (1987) Slipped strand mispairing: a major mechanism for DNA sequence evolution. Mol Biol Evol 4:203–221PubMedGoogle Scholar
  34. Livak KL, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2–ΔΔCT method. Methods 25:402–408CrossRefPubMedGoogle Scholar
  35. Locke J, Howard LT, Aippersbach N, Podemski L, Hodgetts RB (1999) The characterization of DINE-1, a short, interspersed repetitive element present on chromosome and in the centric heterochromatin of Drosophila melanogaster. Chromosoma 108:356–366CrossRefPubMedGoogle Scholar
  36. López-Giráldez F, Andres O, Domingo-Roura X, Bosch M (2006) Análisis of carnivore microsatellites and their intimate association with tRNA-derived SINEs. BMC Genomics 7:269CrossRefPubMedGoogle Scholar
  37. Malausa T, Dalecky A, Ponsard S, Audiot P, Streiff R, Chaval Y, Bourguet D (2007) Genetic structure and gene flow in French populations of two Ostrinia taxa: host races or sibling species? Mol Ecol 16:4210–4222CrossRefPubMedGoogle Scholar
  38. Marchler-Bauer A, Anderson JB, Chitsaz F, Derbyshire MK, DeWeese-Scott C, Fong JH, Geer LY, Geer RC, Gonzales NR, Gwadz M, He S, Hurwitz DI, Jackson JD, Ke Z, Lanczycki CJ, Liebert CA, Liu C, Lu F, Lu S, Marchler GH, Mullokandov M, Song JS, Tasneem A, Thanki N, Yamashita RA, Zhang D, Zhang N, Bryant SH (2009) CDD: Specific functional annotation with the conserved domain database. Nucleic Acids Res 37:D205–D210CrossRefPubMedGoogle Scholar
  39. Meglécz E, Pétenian F, Danchin E, D’Acier AC, Rasplus JY, Faure E (2004) High similarity between flanking regions of different microsatellites detected within each of two species of Lepidoptera: Parnassius apollo and Euphydryas aurinia. Mol Ecol 13:1693–1700CrossRefPubMedGoogle Scholar
  40. Meglécz E, Anderson SJ, Bourguet D, Butcher R, Caldas A, Cassel-Lundhagen A, d’Acier AC, Dawson DA, Faure N, Fauvelot C, Franck P, Harper G, Keyghobadi N, Kluetsch C, Muthulakshmi M, Nagaraju J, Patt A, Péténian F, Silvain JF, Wilcock HR (2007) Microsatellite flanking region similarities among different loci within insect species. Insect Mol Biol 16:175–185CrossRefPubMedGoogle Scholar
  41. Miao XX, Xub SJ, Ming JL, Li MW, Huang JH, Dai FY, Marino SW, Mills DR, Zeng P, Mita K, Jia SH, Zhang Y, Liu WB, Xiang H, Guo QH, Xu AY, Kong XY, Lin HX, Shi YZ, Lu G, Zhang X, Huang W, Yasukochi Y, Sugasaki T, Shimada T, Nagaraju J, Xiang ZH, Wang SY, Goldsmith MR, Lu C, Zhao GP, Huang YP (2005) Simple sequence repeat-based consensus linkage map of Bombyx mori. Proc Natl Acad Sci USA 45:16303–16308CrossRefGoogle Scholar
  42. Miller WJ, Nagel A, Bachmann J, Bachmann L (2000) Evolutionary dynamics of the SGM transposon family in the Drosophila obscura species group. Mol Biol Evol 17:1597–1609PubMedGoogle Scholar
  43. Mita K, Kasahara M, Sasaki S, Nagayasu Y, Yamada T, Kanamori H, Namiki N, Kitagawa M, Yamashita H, Yasukochi Y, Kadono-Okuda K, Yamamoto K, Ajimuar M, Ravikumar G, Shimomura M, Nagamura Y, Shin-I T, Abe H, Shimada T, Morishita S, Sasaki T (2004) The genome sequence of silkworm, Bombyx mori. DNA Res 11:27–36CrossRefPubMedGoogle Scholar
  44. Pemberton JM, Slate J, Bancroft DR, Barrett JA (1995) Nonamplifying alleles at microsatellite loci—a caution for parentage and population studies. Mol Ecol 4:249–252CrossRefPubMedGoogle Scholar
  45. Petersen G, Seberg O (2000) Phylogenetic evidence of excision of stowaway miniature inverted-repeat transposable elements in Triticeae (Poaceae). Mol Biol Evol 17:1589–1596PubMedGoogle Scholar
  46. Posey JE, Pytlos MJ, Sinden RR, Roth DB (2006) Target DNA structure plays a crucial role in RAG transposition. PLoS Biol 4:E350CrossRefPubMedGoogle Scholar
  47. Poulter RT (2003) Vertebrate Helitrons and other novel Helitrons. Gene 313:201–212CrossRefPubMedGoogle Scholar
  48. Prasad MD, Muthulakshmi M, Madju M, Archak S, Mita K, Nagaraju J (2005) Survey analysis of microsatellites in the Silkworm, Bombyx mori: freqeuncy distribution, mutations, marker potential and their conservation in heterologous species. Genetics 169:197–214CrossRefPubMedGoogle Scholar
  49. Quesneville H, Nouaud D, Anxolabéhère D (2006) P elements and MITE relative in the whole genome sequence of Anopheles gambiae. BMC Genomics 7:214CrossRefPubMedGoogle Scholar
  50. Ramsey L, Macaulay M, Cardle L, Morgante M, degli Ivanissevich S, Maestri E, Powell W, Waugh R (1999) Intimate association of microsatellite repeats with retroelements and other dispersed repetitive elements in barley. Plant J 17:415–425CrossRefGoogle Scholar
  51. Reddy KD, Abraham EG, Nagaraju J (1999) Microsatellites in the silkworm, Bombyx mori: abundance, polymorphism, and strain characterization. Genome 42:1057–1065CrossRefPubMedGoogle Scholar
  52. Roeder GS, Rose AB, Pearlman RE (1985) Transposable element sequences involved in the enhancement of yeast gene expression. Proc Natl Acad Sci USA 82:5428–5432CrossRefPubMedGoogle Scholar
  53. Rozen S, Skaletsky HJ (2000) Primer3 on the WWW for general users and for biologist programmers. In: Krawetz S, Misener S (eds) Bioinformatics methods and protocols: methods in molecular biology. Humana Press, Totowa, NJ, pp 365–386Google Scholar
  54. Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: molecular evolutionary genetic analysis (MEGA) software version 4.0. Mol Biol Evol 24:1596–1599CrossRefPubMedGoogle Scholar
  55. Tautz D (1989) Hypervariability of simple sequences as a general source for polymorphic DNA markers. Nucleic Acids Res 17:6463–6471CrossRefPubMedGoogle Scholar
  56. Temnykh S, DeClerck G, Lukashova A, Lipovich L, Cartinhour S, McCouch S (2001) Computational and experimental analysis of microsatellites in rice (Oryza sativa L.): frequency, length variation, transposon associations, and genetic marker potential. Genome Res 11:1441–1452CrossRefPubMedGoogle Scholar
  57. The International Silkworm Genome Consortium (2008) The genome of a lepidopteran model insect, the silkworm Bombyx mori. Insect Biochem Mol Biol 38:1036–1045CrossRefGoogle Scholar
  58. Tu Z (1997) 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 94:7475–7480CrossRefPubMedGoogle Scholar
  59. Tu Z (2000) Molecular and evolutionary analysis of two divergent subfamilies of a novel miniature inverted repeat transposable element in the yellow fever mosquito, Aedes aegypti. Mol Biol Evol 17:1313–1325PubMedGoogle Scholar
  60. Van’t Hof AE, Brakefield PM, Saccheri IJ, Zwaan BJ (2007) Evolutionary dynamics of multilocus microsatellite arrangements in the genome of the butterfly Bicyclus anynana, with implications for other Lepidoptera. Heredity 98:320–328CrossRefPubMedGoogle Scholar
  61. Vivas MV, Garcia-Planells J, Ruiz C, Marfany G, Paricio N, Gonzalez-Duarte R, de Frutos R (1999) GEM, a cluster of repetitive sequences in the Drosophila subobscura genome. Gene 229:47–57CrossRefPubMedGoogle Scholar
  62. Wang J, Wong GK, Ni P, Han Y, Huang X, Zhang J, Ye C, Zhang Y, Hu J, Zhang K et al (2002) RePS: a sequence assembler that masks exact repeats identified from the shotgun data. Genome Res 12:824–831CrossRefPubMedGoogle Scholar
  63. Wang J, Xia Q, He X, Dai M, Ruan J, Chen J, Yu G, Yuan H, Hu Y, Li R, Feng T, Ye C, Lu C, Wang J, Li S, Wong GKS, Yang H, Wang J, Xiang Z, Zhou Z, Yu J (2005) SilkDB: a knowledgebase for silkworm biology and genomics. Nucleic Acids Res 33:D399–D402CrossRefPubMedGoogle Scholar
  64. Weber JL, May PE (1989) Abundant class of human DNA polymorphisms which can be typed using the polymerase chain reaction. Am J Hum Genet 44:388–396PubMedGoogle Scholar
  65. Wessler SR, Bureau TE, White SE (1995) LTR-retrotransposons and MITEs: important players in the evolution of plant genomes. Curr Opin Genet Dev 5:814–821CrossRefPubMedGoogle Scholar
  66. Wicker T, Guyot R, Yahiaoui N, Keller B (2003) CACTA transposons in Triticeae. A diverse family of high-copy repetitive elements. Plant Phys 132:52–63CrossRefGoogle Scholar
  67. Wilder J, Hollocher H (2001) Mobile elements and the genesis of microsatellites in dipterans. Mol Biol Evol 18:384–392PubMedGoogle Scholar
  68. Witte CP, Le QH, Bureau T, Kumar A (2001) Terminal-repeat retrotransposons in miniature (TRIM) are involved in restructuring plant genomes. Proc Natl Acad Sci USA 98:13779–13783CrossRefGoogle Scholar
  69. Xia Q, Zhou Z, Lu C, Cheng D, Dai F, Li B, Zhao P, Zha X, Cheng T, Chai C, Pan G, Xu J, Liu C, Lin Y et al (2004) A draft sequence for the genome of the domesticated silkworm (Bombyx mori). Science 306:1937–1940CrossRefPubMedGoogle Scholar
  70. Yandava CN, Gastier JM, Pulido JC, Brody T, Sheffield V, Murray J, Buetow K, Duyk GM (1997) Characterization of Alu repeats that are associated with trinucleotide and tetranucleotide repeat microsatellites. Genome Res 7:716–724PubMedGoogle Scholar
  71. Yang HP, Barbash DA (2008) Abundant and species-specific DINE-1 transposable elements in 12 Drosophila genomes. Genome Biol 9:R39CrossRefPubMedGoogle Scholar
  72. Yang HP, Hung TL, You TL, Yang TH (2006) Genome-wide comparative analysis of the highly abundant transposable element DINE-1 suggests a recent transpositional burst in Drosophila yakuba. Genetics 173:189–196CrossRefPubMedGoogle Scholar
  73. Zhang DX (2004) Lepidopteran microsatellite DNA: redundant but promising. Trends Ecol Evol 19:507–509CrossRefPubMedGoogle Scholar
  74. Zhou Q (2006) Helitron transposons on the sex chromosome of the platyfish Xiphphorus maculates and their evolution in animal genomes. Zebrafish 3:39–52CrossRefPubMedGoogle Scholar
  75. Zuker M (2003) Mfold web server for nucleic acid folding and hybridization prediction. Nucleic Acids Res 31:3406–3415CrossRefPubMedGoogle Scholar
  76. Zuliani G, Hobbs H (1990) A high frequency of length polymorphisms in repeated sequences adjacent to Alu sequences. Am J Hum Genet 46:963–969PubMedGoogle Scholar

Copyright information

© US Government 2010

Authors and Affiliations

  • Brad S. Coates
    • 1
    Email author
  • Douglas V. Sumerford
    • 1
    • 2
  • Richard L. Hellmich
    • 1
    • 2
  • Leslie C. Lewis
    • 1
    • 2
  1. 1.USDA-ARS, Corn Insect and Crop Genetics Research Unit, 113 Genetics LabIowa State UniversityAmesUSA
  2. 2.Department of EntomologyIowa State UniversityAmesUSA

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